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Changes in fetal blood flow in hypoxemia during labor

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Changes in fetal blood flow in hypoxemia during labor
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  Ultrasound Obstet Gynecol   2009;  34 : 177–181Published online 8 July 2009 in Wiley InterScience (www.interscience.wiley.com).  DOI:  10.1002/uog.6420 Pulsations in the umbilical vein during labor are associatedwith increased risk of operative delivery for fetal distress G. S. GHOSH, J. FU, P. OLOFSSON and S. GUDMUNDSSON Lund University, Department of Obstetrics and Gynecology, Malm¨ o University Hospital, Malm¨ o, Sweden KEYWORDS : cardiotocography; Doppler; hypoxia; intrapartum; labor; pregnancy; pulsation; ultrasound; umbilical vein ABSTRACT Objectives  Underphysiologicalconditionsthebloodflowvelocity waveform in the umbilical vein (UV) has aneven non-pulsating pattern. Pulsations in the UV havebeen described in human fetuses exposed to chronichypoxia and heart failure. Current techniques for fetal surveillance during labor and delivery involve a risk of both over- and underestimation of fetal hypoxia. Weaimed to examine whether pulsations in the UV appear inthe human fetus during suspected intrapartum hypoxia,and if so whether they are associated with increased riskof operative delivery for fetal distress (ODFD).  Methods  This was a prospective double blind studyincluding 52 normal pregnancies. A Doppler examinationof the UV was performed on 26 fetuses with pathological and 26 fetuses with normal cardiotocography (CTG)during labor. Presence or absence of pulsations in theUV were noted and related to perinatal outcome.  Results  Pulsations in the UV were seen in eight (30.8%)of the fetuses with pathological CTG, of which six (75%)underwent ODFD. No pulsations were seen in the other18(69.2%)fetuseswithpathologicalCTGandthesewereall delivered without ODFD. No pulsations were seen inthe UV in the fetuses with normal CTG and these wereall delivered without ODFD. Among the fetuses with pathological CTG, there was an increased risk of ODFDin fetuses with vs. those without pulsations in the UV (  P  <  0 . 0001). Conclusions  Pulsations in the UV can be observed inhuman fetuses during suspected intrapartum hypoxiaand these pulsations are associated with an increased risk of ODFD. Doppler examination of the UV might  give important additional information on fetal conditionduring labor and delivery. Copyright   ©  2009 ISUOG.Published by John Wiley & Sons, Ltd. INTRODUCTION The umbilical vein (UV) provides the fetus with well-oxygenated blood from the placenta. Under normalcircumstances 20–30% of the blood bypasses the liverand is shunted through the ductus venosus to supplythe fetal heart and brain 1 , 2 . In the chronically hypoxicfetus, such as the intrauterine growth-restricted (IUGR)fetus 3–5 , the ductus venosus dilates and the blood volumeshunted through the ductus venosus increases to maintainadequate oxygenation of these vital organs 6–9 .Under physiological conditions a Doppler ultrasoundexamination of the UV will show an even, non-pulsatingblood flow velocity pattern 1 , since the pulse waves causedby atrial contractions are not propagated backwardsthrough the narrow ductus venosus. However, if theductus venosus widens, the pulse waves might propagateinto the UV andresult ina pulsating pattern.Pulsations inthe UV were first described by Lingman  et al  . 10 in fetusesin imminent danger of asphyxia and later by Gudmunds-son  et al  . 11 in fetuses that were hydropic due to heartfailure. Pulsations in the UV have been found in rela-tion to increased central venous pressure in hypoxia 12 , 13 and heart failure 13 . In 1998, Bellotti  et al  . 14 reported twoIUGR fetuses with dilatation of the ductus venosus andpulsations in the blood flow velocity waveform of theUV. Many authors thereafter reported on UV pulsationsin fetuses exposed to chronic hypoxia which had pooroutcome 15 , 16 . To our knowledge, there have been nostudies performed to examine whether pulsations in theUV appear during intrapartum fetal hypoxia.Current techniques for fetal surveillance during laborand delivery consist of mainly cardiotocography (CTG),ST-analysis ofthe fetalECG(STAN)andfetalscalpbloodsampling. These techniques involve a risk of both over-and underestimation of fetal hypoxia, with unnecessaryoperative intervention and/or hypoxic injury to the fetusas possible consequences 17 . Correspondence to:  Dr G. S. Ghosh, Lund University, Department of Obstetrics and Gynecology, Malm ¨o University Hospital, SE-20502Malm ¨o, Sweden (e-mail: gisela.ghosh@med.lu.se) Accepted: 15 January 2009 Copyright © 2009 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER  178  Ghosh et al. The aim of this study, therefore, was to examinewhether pulsations in the UV appear in the human fetusduring suspected intrapartum hypoxia, and if so wetherthey are associated with increased risk for operativedelivery for fetal distress (ODFD). PATIENTS AND METHODS This prospective double blind study was carried out at thematernity unit at Malm ¨o University Hospital. It includedwomen with pregnancies of   ≥ 37 weeks’ gestation witha singleton fetus in cephalic presentation and in activelabor. All women had been dated by an early ultrasoundexamination and had had a normal pregnancy course.Active labor was defined as regular contractions with adilation of the cervix of 3–10 cm. Women in the secondstage of labor were not included. Intrapartum Dopplerexaminations of the UV were performed in 26 fetuseswith pathological and 26 fetuses with normal CTG.CTG was classified as pathological in the presence of:repeated late decelerations ( n = 12), repeated variabledecelerations with a duration of   > 60 s ( n = 12), orfetal heart rate  > 180 bpm in addition to pathologicalvariability (variability in rate of   < 5 or  > 25 bpm)( n = 2) 18 . In most cases of pathological CTG, when noimmediateinterventionwasrequired,thefetalsurveillancewas intensified by fetal scalp pH/lactate samplings andSTAN. Informed consent was obtained from all womenand Doppler examination was approved by the localethics committee. The women were enrolled into thestudy provided that the examiner was not on active dutyin the labor ward (so as to keep the study blind) and thatno immediate intervention was required. Three womendeclined to participate in the study and four cases werenot included as immediate intervention was required.Doppler blood flow velocity examination was per-formedin the UV, both inthe intra-abdominalpart and inthe umbilical cord. With the women in a supine position,a two-dimensional color Doppler technique (GE VolusonI, GE Healthcare, Milwaukee, WI, USA or Acuson D 50,Acuson, Mountain View, CA, USA) was used to identifythe UV. The intra-abdominal recording was made in themiddle portion of the UV, between the abdominal walland the ductus venosus. The umbilical cord recording wasmade in a free-floating central loop of the cord. The angleofinsonationwas < 30 ◦ andatleasteightheartcycleswereincluded. Recordings were performed during the pausebetween uterine contractions, in the absence of maternaland fetal breathing or other movements. The presence orabsence of pulsations in the UV blood velocity waveformwas noted. In all cases of UV pulsations a reduction of the maximum blood velocity of 15% or more was noted.The outcome of the Doppler recordings was not disclosedto the managing obstetrician, the midwife or the patient.We compared the UV Doppler results to the perinataloutcome, including birth weight and numbers of babiesthatweresmall-for-gestationalage(SGA)(definedasbirthweight  ≤− 2 SD of mean birth weight for gestationalage), Cesarean sections and operative deliveries for fetaldistress (ODFD), pH in arterial and venous umbilicalblood, Apgar score and numbers admitted to the neonatalintensive care unit (NICU).ODFD was defined as deliveryby Cesarean section, vacuum extraction or forceps dueto suspected fetal distress. Fisher’s exact test was usedfor nominal variables and Wilcoxon’s rank sum test forcontinuous variables. A  P -value of   < 0 . 05 was consideredstatistically significant. RESULTS A comparison of demographics and perinatal outcomebetween the group with and that without pathologicalCTG is shown in Table 1. Among patients with apathological CTG tracing, rupture of the membranes,meconium-stained amniotic fluid, oxytocin infusion andepidural anesthesia were more common than they were inpatients with a normal CTG tracing.Pulsations in the intra-abdominal part of the UVwere seen in eight (30.8%) of the 26 patients withpathological fetal CTG. Six (75.0%) of these eightpatients underwent ODFD (two Cesarean sections andfour vacuum extractions), one of whom had presentedon the labor ward with late decelerations and reducedvariability on CTG. The decision to deliver the patientby emergency Cesarean section was made a few minutesafter the Doppler examination was performed. In anothercase, CTG showed late decelerations. Repeated fetal scalplactate sampling showed increasing levels of lactate andthe decision to deliver the baby by emergency Cesareansection was made approximately half an hour after theDoppler examination. In two cases the CTG showed latedecelerations and a decision to deliver the patients byvacuum extraction was made shortly after the Dopplerexamination. In one case the fetal heart rate was 180 bpmwith a variability of   < 5 bpm. STAN showed repeatedsignificant ST-events and a decision to deliver the babyby vacuum extraction was made shortly after the Dopplerexamination. In the last case of ODFD, CTG showedlate decelerations at the time of Doppler examination.CTG improved somewhat shortly after the examination,but 1 h later CTG showed bradycardia, with a fetalheart rate of 50–60 bpm. The baby was delivered byvacuum extraction. One baby was born with a low Apgarscore (2, 5 and 9 at 1, 5 and 10 min, respectively),one with low umbilical artery pH (7.05) and two withlow UV pH (7.13 and 7.11). No baby was admittedto the NICU. Fetuses with UV pulsations underwentODFD more often than did fetuses without UVpulsations( P  <  0 . 0001) (Table 1). Two fetuses with UV pulsationshad a spontaneous vaginal delivery. In both cases theCTG tracing was pathological at the time of the Dopplerexamination, but improved later during labor. Repeatedfetal scalp lactate samples were normal and the womendelivered healthy babies, one 7 and one 5 hours later. TheApgarscoresandpHoftheumbilicalarteryandveinwerenormal in both cases.With respect to type of CTG abnormality (latedecelerations ( n = 12), variable decelerations ( n = 12) Copyright © 2009 ISUOG. Published by John Wiley & Sons, Ltd.  Ultrasound Obstet Gynecol   2009;  34 : 177–181.   U V  p u l    s  a t   i    on s  d  u r  i   n  g l    a b   o r  1   7   9   Table 1  Demographics and perinatal outcome of the study groups P Pathological CTG UV puls. vs. UV puls. vs.Normal vs. no UV puls. no UV puls.Normal CTG All No UV puls. UV puls. pathol. CTG (pathol. CTG) (all CTG) n  26 26 18 8UV puls. intra-abdominal 0 8 0 8UV puls. in umbilical cord 0 0 0 0GA (weeks) 40.0 (37–42) 40.0 (37–43) 40.0 (37–43) 41.0 (39–43) NS NS NSNulliparous 17 (65.4) 18 (69.2) 13 (72.2) 5 (62.5) NS NS NSExamination to delivery time (min) 212 (30–805) 127 (8–614) 166.5 (66–614) 43.5 (8–426) NS NS NSCervical dilation (cm) 4.0 (3–10) 6.0 (3–10) 6.5 (3–10) 4.5 (3–10) NS NS NSRuptured membranes 15 (57.7) 25 (96.1) 17 (94.4) 8 (100)  < 0 .003 NS NSMeconium-stained amniotic fluid 1 (3.8) 14 (53.8) 8 (44.4) 6 (75.0)  < 0 .0002 NS  < 0 .005Epidural analgesia 0 15 (57.7) 12 (66.7) 3 (37.5)  < 0 .0001 NS NSOxytocin infusion 1 (3.8) 9 (34.6) 7 (38.9) 2 (25.0)  < 0 .02 NS NSBirth weight (g) 3620 (2530–4675) 3657 (2745–4050) 3507 (2745–4050) 3845 (3355–4035) NS  < 0 .05 NSSGA 0 0 0 0 NS NS NSCesarean section 0 5 (19.2) 3 (16.7) 2 (25.0) NS NS NSODFD 0 6 (23.1) 0 6 (75.0)  < 0 .03  < 0 .0001  < 0 .0001pH umbilical artery  < 7 . 1  0 2/19 (10.5) 1/14 (7.1) 1/5 (20.0) NS NS NSpH umbilical vein  < 7 . 2  0 6 (23.1) 4 (22.2) 2 (25.0)  < 0 .03 NS NS5-min Apgar score  < 7  0 2 (7.7) 1 (5.6) 1 (12.5) NS NS NSNICU 1 (3.8) 1 (3.8) 1 (5.6) 0 NS NS NSData are presented as  n  (%) or median (range). CTG, cardiotocography; GA, gestational age; NICU, neonatal intensive care unit; NS, non-significant; ODFD, operative delivery for fetal distress;pathol., pathological; puls., pulsations; SGA, small for gestational age; UV, umbilical vein.  C o  p  yr i     gh   t    © 2  0  0  9 I   S   U O G .P  u b  l   i    s h   e  d   b    y  J   oh  n Wi   l    e   y & S   on s  ,L  t   d   .  U l    t   r  a s  oun d   O b   s  t   e  t   G  yn e  c  o l    2  0  0  9  ;   3  4    : 1  7  7 –1  8 1  .  180  Ghosh et al. and tachycardia ( n = 2)), UV pulsations were detectedin six, one and one case, respectively, and ODFD wasperformed in five, no and one case, respectively.No pulsations were seen in 18 of the fetuses withpathological CTG. Three of these fetuses were deliveredby Cesarean section and three by vacuum extraction duetoprolongedlabor.NoODFDwereperformed.Onebabywas referred to the NICU due to neonatal pulmonarymaladaptation. This baby had an Apgar score of 4, 7 and8at1,5and10 mins,respectively,andanUVpHof 7.28.Analysis of the umbilical artery pH failed. The baby wasdischarged from the NICU within 2 days (Table 1).UV pulsations were not seen in the umbilical cord inany of the fetuses with pathological CTG.UV pulsations were not seen in any of the fetuseswith a normal CTG tracing, regardless of the site of therecording. All of these babies were delivered vaginally,three by vacuum extraction due to prolonged labor. NoODFD were required. One baby was admitted to theNICU due to pulmonary maladaptation (Table 1). DISCUSSION The results of this observational study indicate that usingUV Doppler examination as part of the intrapartumsurveillance of fetuses with suspected distress might giveadditional useful information about the fetal condition.Fetuses with pulsations in the UV had an increasedrisk of ODFD, even though only half of the newbornsdelivered by ODFD showed signs of hypoxia at birth.How this should be interpreted is not clear. One mightspeculate that a pulsating blood flow pattern in the intra-abdominalpartoftheUVmightbeanearlycompensatorymechanism reflecting the effect of hypoxia either on theheart, ductus venous or both. Automatic redistribution of fetal circulation might maintain cord blood gases withinnormal limits for some time 19 .Surveillance for detection of fetal hypoxia during laboris currently based on CTG, STAN and fetal blood sam-pling. The introduction of CTG reduced the rate of neonatal seizures at the cost of an increased rate of intra-partum Cesarean section. Interpretation of CTG requiresexperience and involves the risk of both false-positiveas well as false-negative results 20 . Surveillance by STANimproves the possibility of identifying fetal hypoxia. Aconsequent reduction of both metabolic acidosis andODFD has been demonstrated 21 . Fetal scalp pH/lactatesamplesprovideanopportunitytoobtainadditionalinfor-mation about the fetal condition. However, the samplecan be difficult to obtain and the result provided givesonly momentary information about the fetal condition 22 .Repeated samplings might therefore be necessary.Pulsations in the UV might occur in various situations.In early pregnancy, UV pulsations are normally seen dueto the small diameter of the vessel. Provided there isnormal development of the placenta, these pulsationsdisappear at around 13 weeks of gestation 23 . Chronichypoxia has been associated with pulsations in the UV,as a result either of dilatation of the ductus venosusor of myocardial decompensation and increased centralvenous pressure 12 , 24 . In 1986, Lingman  et al  . 10 foundUV pulsations in 27% fetuses which were later deliveredby emergency Cesarean section due to changes in theCTG. Kiserud  et al  . 25 showed that 30% of severely IUGRfetuses have a pulsating blood flow pattern in the UV.UV pulsations have also been described by Tulzer  et al  . 13 as a sign of fetal heart failure in non-immune hydropicfetuses. Our study, however, was performed on low-riskpregnancies and none of the babies was SGA. Thus, therisk of chronic hypoxia or heart failure as an explanationfor pulsations in the Doppler waveform of the UV musthave been minimal.Compared with patients with a normal CTG, thosewith a pathological CTG tracing were found to haverupture of the fetal membranes, meconium staining of theamniotic fluid, oxytocin infusion and epidural anesthesiamore often. The higher frequency of cases with rupturedmembranes is probably explained by the necessity of internal electronic fetal monitoring and/or fetal scalpsamples in cases with a suspected pathological CTGtracing.Thehigher frequencyof meconiumstaining of theamnioticfluidwasanexpectedfinding,asthisisassociatedwith signs of hypoyxia during labor and delivery 26 . Themore common use of oxytocin infusion and epiduralanesthesia might be an indication of a protracted courseof labor 27 ; this, however, was not analyzed in the presentstudy.Pulsating venous blood flow pattern in the umbilicalcord was not observed in any fetus. In our experience, agradual deterioration in the venous blood flow pattern isseen in fetuses exposed to chronic hypoxia. In most cases,the diastolic part of the blood flow velocity waveform inthe ductus venosus is the first to be affected. Thereafter,pulsations in the intra-abdominal part of the UV appear.Pulsations in the umbilical cord are only observed in themost severe cases. Whether the same progression occursin fetuses exposed to acute hypoxia is not clear, butthis could offer a possible explanation for the absence of pulsations in the umbilical cord seen in this study.Recording of blood velocities in the UV is easy toperform, even during labor. Doppler examination of theductus venosus might provide more information aboutthe fetal condition, but this technique is more difficultto perform and, due to the small caliber of the vessel,it is more sensitive to fetal and maternal movements.All women in the present study were in active laborand the short time span between the painful uterinecontractions limited the time for examination. Time wasalso limited due to severity of the pathological CTGtracings. Therefore, Doppler examination of the ductusvenosus was not included in the study.We are aware that the number of cases included in thisstudy was small. Pathological CTG occurs infrequentlyduring labor in otherwise normal pregnancies, makingthe recruitment of patients difficult. Only three womendeclined to participate in the study, but in some casesthe severity of the CTG pattern required immediateintervention, leaving no time for a Doppler examination. Copyright © 2009 ISUOG. Published by John Wiley & Sons, Ltd.  Ultrasound Obstet Gynecol   2009;  34 : 177–181.  UV pulsations during labor  181 The results of this pilot study need to be tested in aprospective randomized controlled study.Intrapartum Doppler studies have been performedon other vessels with various results. Maesel  et al  . 28 examinedthe middlecerebralartery(MCA) incorrelationto mode of delivery and found a significantly lowerpulsatility index in the MCA of SGA babies delivered byCesareansectioncomparedwiththosedeliveredvaginally.Furthermore, intrapartum umbilical artery Doppler hasbeen shown by several authors 29 , 30 to be a poor predictorof adverse perinatal outcome.The results from this study show an increased risk of ODFD in fetuses with UV pulsations and pathologicalCTG tracing. Absence of pulsations in the UV might bea reassuring sign. However, it is important to rememberthatDopplerexaminationoftheUVprovidesinformationabout a compensatory mechanism in the fetal circula-tion and not about the oxygen levels in the fetal blood.Equally important is to notice that the fetal conditionmight deteriorate fast and a normal Doppler examinationmust continuously be re-evaluated in relation to otherparameters of fetal surveillance.In conclusion, the results of this study show thatpulsations in the UV could be seen in fetuses duringsuspected intrapartum hypoxia in otherwise normalpregnancies. Pulsations in the UV in these fetuses wereassociated with an increased risk of ODFD. Dopplerexamination of the UV might contribute importantadditional information about the fetal condition. REFERENCES 1. Kiserud T. Fetal venous circulation–an update on hemodynam-ics.  J Perinat Med   2000;  28 : 90–96.2. Kiserud T, Rasmussen S, Skulstad SM. 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