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OBSTETRICS
Predictable progressive Doppler deterioration in
IUGR: does it really exist?
Julia Unterscheider, MD; Sean Daly, MD; Michael Patrick Geary, MD; Mairead Mary Kennelly, MD;
Fionnuala Mary McAuliffe, MD; Keelin O’Donoghue, PhD; Alyson Hunter, MD; John Joseph Morrison, MD;
Gerard Burke, FRCOG; Patrick Dicker, PhD; Elizabeth Catherine Tully, PhD; Fergal Desmond Malone, MD

OBJECTIVE: An objective of the Prospective Observational Trial to had an abnormal UA, 300 (27%) had an abnormal MCA, and 129
Optimize Pediatric Health in IUGR (PORTO) study was to evaluate (11%) had an abnormal DV Doppler. The classic pattern from
multivessel Doppler changes in a large cohort of intrauterine growth abnormal UA to MCA to DV existed but no more frequently than any of
restriction (IUGR) fetuses to establish whether a predictable progres- the other potential pattern. Doppler interrogation of the UA and MCA
sive sequence of Doppler deterioration exists and to correlate these remains the most useful and practical tool in identifying fetuses at
Doppler findings with respective perinatal outcomes. risk of adverse perinatal outcome, capturing 88% of all adverse
outcomes.
STUDY DESIGN: More than 1100 unselected consecutive ultrasound-
dated singleton pregnancies with estimated fetal weight (EFW) less CONCLUSION: In contrast to previous reports, we have demonstrated
than the 10th centile were recruited between January 2010 and June multiple potential patterns of Doppler deterioration in this large
2012. Eligible pregnancies were assessed by serial Doppler interro- prospective cohort of IUGR pregnancies, which calls into question
gation of umbilical (UA) and middle cerebral (MCA) arteries, ductus the usefulness of multivessel Doppler assessment to inform fre-
venosus (DV), aortic isthmus, and myocardial performance index (MPI). quency of surveillance and timing of delivery of IUGR fetuses. These
Intervals between Doppler changes and patterns of deterioration were data will be critically important for planning any future intervention
recorded and correlated with respective perinatal outcomes. trials.
RESULTS: Our study of 1116 nonanomalous fetuses comprised 7769 Key words: Doppler, intrauterine growth restriction, sequential
individual Doppler data points. Five hundred eleven patients (46%) changes, umbilical artery

Cite this article as: Unterscheider J, Daly S, Geary MP, et al. Predictable progressive Doppler deterioration in IUGR: does it really exist? Am J Obstet Gynecol 2013;209:539.e1-7.

A progressive predictable sequence


of placental and fetal Doppler
changes has been described as an adaptive
The surveillance and management of
IUGR secondary to placental dysfunction
is facilitated by umbilical artery (UA)
Several studies have contributed to the
understanding of longitudinal Doppler
changes occurring in IUGR.4-6 Knowl-
mechanism to a suboptimal intrauterine Doppler assessment, and this is widely edge about temporal deterioration in
environment in pregnancies affected by accepted as the primary ultrasound sur- maternal and fetal vessels is desired to
intrauterine growth restriction (IUGR). veillance tool in such pregnancies.1-3 inform frequency of surveillance and

From the Departments of Obstetrics and Gynecology (Drs Unterscheider, Tully, and Malone) and Epidemiology and Public Health (Dr Dicker), Royal
College of Surgeons in Ireland; Department of Obstetrics and Gynecology (Dr Daly) and University College Dublin Center for Human Reproduction
(Dr Kennelly), Coombe Women and Infants University Hospital; Department of Obstetrics and Gynecology, Rotunda Hospital (Dr Geary); Department
of Obstetrics and Gynecology, University College Dublin School of Medicine and Medical Science, National Maternity Hospital (Dr McAuliffe); and
Departments of Obstetrics and Gynecology, University College Cork, Cork University Maternity Hospital, Cork (Dr O’Donoghue); Royal Jubilee Maternity
Hospital, Belfast (Dr Hunter); National University of Ireland, Galway (Dr Morrison); and Graduate Entry Medical School, University of Limerick, Limerick
(Dr Burke), Ireland.
Received May 30, 2013; revised Aug. 12, 2013; accepted Aug. 27, 2013.
The Prospective Observational Trial to Optimize Pediatric Health in IUGR Study was conducted by the Perinatal Ireland Research Consortium, a
nationwide collaborative research network comprising the 7 largest academic obstetric centers in Ireland. The study was funded by the Health Research
Board and Friends of the Rotunda.
The authors report no conflict of interest.
Presented at the 33rd annual meeting of the Society for Maternal-Fetal Medicine, San Francisco, CA, Feb. 11-16, 2013.
Reprints: Julia Unterscheider, MD, Department of Obstetrics and Gynecology, Royal College of Surgeons in Ireland, Rotunda Hospital, Parnell Square,
Dublin 1, Ireland. juliaunterscheider@rcsi.ie.
0002-9378/$36.00  ª 2013 Mosby, Inc. All rights reserved.  http://dx.doi.org/10.1016/j.ajog.2013.08.039

See Journal Club, page 589

DECEMBER 2013 American Journal of Obstetrics & Gynecology 539.e1


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optimal surveillance of fetuses with an


TABLE estimated fetal weight (EFW) less than
Maternal demographics and fetal characteristics (n [ 1116) the 10th centile.10 The objective of this
Characteristic n (%)/mean ± SD particular analysis was to study Doppler
Age, y 30  6 changes in multiple vessels including
UA, MCA, DV, AoI, and myocardial
Ethnicity (white European) 907 (83%)
performance index (MPI) and to estab-
Spontaneous conception 1100 (99%) lish whether a predictable progressive
Maternal height, cm 162  12 sequence of Doppler deterioration exists
Maternal weight at booking, kg 64  13 at the level of the individual fetus and
to determine any added benefit in ap-
BMI, kg/m 2
24.1  4.7
plying these Doppler assessments in
Smokers 261 (23%) IUGR informing surveillance intervals
Hypertensive disease/preeclampsia 134 (12%) and timing of delivery.
GA at enrolment, wks 30.1  3.9
M ATERIALS AND M ETHODS
GA at delivery, wks 37.8  3.0 The PORTO trial is a multicenter pro-
Weight at delivery, g 2495  671 spective study conducted at 7 academic
NICU admission 312 (28%) obstetric centers in Ireland. For the
purpose of the study, IUGR was defined
Adverse perinatal outcome 57 (5%)
as an EFW below the 10th centile based
Apgar score <7 5
13 (1%) on sonographic measurements of fetal
Stillbirths 3 (1:370) biparietal diameter, head circumference,
Neonatal deaths 3 (1:370) abdominal circumference, and femur
Continuous variables are summarized with mean  SD and categorical variables with n (percentage).
length (Hadlock-4).11
BMI, body mass index; GA, gestational age; NICU, neonatal intensive care unit.
Between January 2010 and June 2012,
Unterscheider. Doppler deterioration in IUGR. Am J Obstet Gynecol 2013.
the PORTO study recruited 1200 co-
nsecutive ultrasound-dated singleton
pregnancies. Dating occurred either by
timing of delivery. However, these the pulmonary and aortic outflow tracts, crown-rump length measurement prior
studies have been either retrospective and finally (7) reversed a-wave in the DV.4 to 14 weeks’ gestation or by composite
or comprised small patient numbers. These compensatory and decompen- measurement of biparietal diameter
Furthermore, it is important to note that satory changes have resulted in debate on (BPD), head circumference, abdominal
in fact most of these papers describing a the benefit of assessing vessels other than circumference, and femur length from
temporal sequence refer to Doppler ab- the UA in the setting of IUGR. Although 14 0/7 to 22 0/7 weeks’ gestation. In-
normalities within a population of IUGR some data suggest a role for DV Doppler clusion criteria were a gestation between
fetuses rather than a predictable pro- to inform timing of delivery in severe 24 0/7 and 36 6/7 weeks and an EFW of
gressive sequence occurring within the IUGR, evidence from a large random- 500 g or more. Fetuses with major
individual fetus. It is plausible therefore ized trial is still awaited.7 structural and/ or chromosomal abnor-
that such prior population data may not Similarly, although reports suggest a malities were excluded from the final
actually be applicable to the longitudinal role for abnormal aortic isthmus (AoI) analysis. Institutional review board
surveillance of the individual fetus in Doppler in the setting of IUGR,8 the approval was obtained at each partici-
clinical practice. recently published Society for Maternal- pating site, and all study participants
Longitudinal cumulative-onset time Fetal Medicine clinical guideline on gave written informed consent.
curves of Doppler abnormalities des- Doppler assessment of the IUGR fetus9 Referral for consideration for enroll-
cribing a time-dependent change of states that Doppler studies other than ment to the study occurred if small fetal
various vessels are thought to follow one the UA should be reserved solely for size was suspected because of clinical
certain predictable pattern from the research protocols. The same guideline evaluation in the antenatal setting.
following: (1) abnormal blood flow in the acknowledges that there “does appear to A PORTO research sonographer then
uterine arteries, (2) increased resistance in be a natural progression of changes in confirmed that the EFW was below the
the umbilical arteries, (3) compensatory the Doppler of UA, MCA, and DV with 10th centile and performed a detailed
flow in the middle cerebral artery (MCA) a large variability in manifestation.” evaluation of the fetal anatomy and
indicating cerebral redistribution, (4) ab- The goal of the prospective multi- uterine artery Doppler at enrollment. All
sent end-diastolic flow in the UA, which center Prospective Observational Trial eligible pregnancies underwent serial
is followed by (5) absent a-wave in the to Optimize Pediatric Health in IUGR sonographic evaluation of fetal weight
ductus venosus (DV), (6) abnormalities in (PORTO) study was to evaluate the at 2 weekly intervals until birth, and

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all normally formed fetuses underwent
evaluation of amniotic fluid volume, FIGURE 1
biophysical profile scoring (BPP), and Cumulative frequencies of Doppler abnormalities (n [ 1116)
multivessel Doppler of the UA, MCA, DV,
AoI, and MPI at every subsequent contact 70 UA
with the research sonographers until de- MCA
livery. This occurred at a minimum of 60 AI
2 weekly intervals but more frequently, DV
MPI
even daily, if deemed necessary. 50
A report of all sonographic findings

Cumulative %
was filed in the patient’s case record and
40
made available to the managing clini-
cian. All prenatal and ultrasound data
were contemporaneously transferred to 30
an ultrasound software system (View-
point; MDI Viewpoint, Jacksonville, FL) 20
and uploaded onto a live web-based
central consolidated database. 10
An abnormal UA Doppler assessment
was defined as a pulsatility index (PI) 0
above the 95th centile, (intermittently)
absent (AEDF) or reversed end-diastolic
-20 -18 -16 -14 -12 -10 -8 -6 -4 -2 0
flow (REDF). MCA abnormalities were
defined as a PI less than the fifth centile.12 Gestational Weeks to Delivery
DV was recorded as being abnormal Figure 1 outlines how long each of the Doppler abnormalities were present prior to delivery,
with a PI greater than the 95th centile, expressed as a cumulative percentage of Doppler abnormalities occurring in the full cohort of 1116
and absent or reversed a-wave flow.13 AoI pregnancies with an EFW less than the 10th centile.
Doppler was considered abnormal ac- EFW, estimated fetal weight.
cording to gestational ageebased refer- Unterscheider. Doppler deterioration in IUGR. Am J Obstet Gynecol 2013.
ence ranges described by Del Rio et al.14
MPI was measured in the left ventricle
assessing individual isovolumetric con-
traction (ICT) and relaxation times (IRT) FIGURE 2
over the period between opening and Mean time-to-delivery interval for each Doppler (n [ 1116)
closure of the semilunar valves (ejection
time [ET]) (ICTþIRT/ET).15 A cere-
broplacental Doppler ratio less than 1 was
considered abnormal.
A small group of 10 research sonog-
raphers performed all Doppler studies.
Initial structured training was provided
by maternal-fetal medicine subspecialists,
and quality assurance assessments with
periodic resubmission of images were
carried out at regular intervals. To mini-
mize the intra- and interobserver vari-
ability, all ultrasound assessments were
carried out by one single sonographer per
center. All data were interpreted using
published, standardized references for
various Doppler findings, therefore elim- Figure 2 outlines the mean time from first Doppler abnormality to delivery for each interrogated
inating misinterpretation of data. vessel: UA, MCA, DV, AoI, and MPI.
In cases of AEDF or REDF in the UA, AoI, abnormal aortic isthmus; DV, ductus venosus; MCA, middle cerebral arteries; MPI, myocardial performance index; UA, umbilical
the patient was admitted to the hospital, arteries.
and a daily computerized short-term Unterscheider. Doppler deterioration in IUGR. Am J Obstet Gynecol 2013.
variation cardiotocograph (CTG) was

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carried out. Corticosteroids for fetal lung


FIGURE 3 maturation were administered between
Doppler deterioration for various sequences (n [ 1116) 24 and 36 weeks’ gestation if delivery
was thought to be likely within 1 week.
The impact of steroid administration on
Doppler variation was not examined.
Decisions relating to timing and mode
of delivery were left to the discretion of
the lead clinician managing each case.
Although such management decisions
were not prespecified by the study design,
there was, however, general agreement
among the clinicians in Ireland to deliver
the AEDF cases by 34 weeks’ gestation.
The tertiary-level neonatal care facilities
were available in all 7 sites.
Pediatric outcomes for infants not
requiring neonatal intensive care were
recorded by the research sonographers
and uploaded onto the database. Infants
requiring neonatal intensive care ad-
mission had their outcomes recorded
by neonatal medical or nursing staff.
Adverse perinatal outcome was defined
as a composite outcome of intraventric-
ular hemorrhage (IVH), periventricular
leukomalacia (PVL), hypoxic ischemic
encephalopathy (HIE), necrotizing en-
terocolitis (NEC), BPD, sepsis, and death.
Given that all study sites were members
of the Vermont Oxford Network,16 defi-
nitions for IVH, PVL, HIE, NEC, BPD,
and sepsis were standardized across all
centers derived from the Vermont Ox-
ford Network manual. The prediction of
adverse outcome was evaluated by any
Doppler abnormality during the study
period.

Use of statistics
Prior to statistical analysis, all ultrasound
and outcome data were screened for
anomalous records or potential outliers
and followed up with sonographers for
resolution. Statistical comparisons were
performed using the c2 test of associa-
tion. SAS version 9.2 (SAS Institute,

)
sequential deterioration for vessels UA/DV/
MCA; and C, pattern 3 describes a sequential
deterioration for vessels MCA/UA/DV.
DV, ductus venosus; MCA, middle cerebral arteries; UA, umbilical
Various patterns of Doppler deterioration occurring in a truly sequential manner are outlined. A, arteries.
Pattern 1 describes a sequential deterioration for vessels UA/MCA/DV; B, pattern 2 describes a Unterscheider. Doppler deterioration in IUGR. Am J Obstet
Gynecol 2013.

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www.AJOG.org Obstetrics Research
Cary, NC) was used for data manage- this represents the main sequence of venosus Doppler. In actual fact, what we
ment and statistical analysis. progressive deterioration at the individ- found was that all 6 possible sequences
ual fetal patient level. of Doppler deterioration were similarly
R ESULTS To emphasize this point further, represented in our dataset.
Of 1200 recruited pregnancies with an Figure 2 represents the mean time from Interestingly, even when we focused
EFW below the 10th centile, 32 (2.7%) first diagnosis of Doppler abnormality on a selected group of 113 fetuses who
were excluded because of chromosomal until delivery. If there was a single had such severe IUGR that required
and/or structural abnormalities, 13 (1%) dominant sequence of deterioration in delivery prior to 34 weeks, we still could
withdrew their consent, and 13 (1%) Doppler abnormalities in the setting of not identify one single predominant
delivered outside Ireland, whereas a IUGR, we would have expected to see a pathway or sequence of deterioration.
further 26 (2.2%) were lost to follow-up. gradual shortening in the time from first Average gestational age at presentation
This resulted in 1116 patients com- diagnosis to delivery for each of the for all 6 Doppler sequences was 24-27
pleting the study protocol. relevant Doppler findings. In contrast, weeks, showing no statistical significance
The mean maternal age was 30 years, what we actually found was no overall when analyzing the progression in rela-
the mean body mass index was 24 kg/m2, pattern of Doppler deterioration in each tion to gestational age at enrollment (P ¼
and the vast majority of women were of of these vessels. For example, although .1835, Kruskal-Wallis test).
white European descent. This is consis- the mean time from diagnosis to delivery Correlation of Doppler findings with
tent with the demographic profile of the for an abnormal UA was 26 days, the respective perinatal morbidity and mor-
overall obstetric population attending for mean time from diagnosis to delivery for tality outcomes shows that an abnormal
antenatal care in Ireland,17 reflecting an abnormal DV was 37 days and 39 days umbilical artery Doppler is by far the
unselected group of recruited pregnan- for an abnormal MPI. most likely test to be associated with
cies. Twenty-three percent were smokers Our data demonstrate that there are in adverse outcome, capturing 86% of all
and 12% were affected by hypertensive fact various patterns of Doppler deterio- recorded adverse outcomes (Figure 5).
disease or preeclampsia. The mean ges- ration occurring in a truly sequential Second, the next most useful vessel is an
tational age (GA) at enrollment to the manner, meaning that an initial abnormal abnormal middle cerebral artery Doppler,
study was 30.1 weeks and the mean GA at Doppler finding was followed by another capturing 51% of all adverse outcomes.
delivery was 37.8 weeks. The Table out- and another in one and the same fetus If significant time and effort are placed
lines maternal demographics and fetal over time. Given that we interrogated into searching for other Doppler abnor-
characteristics. 5 fetal vessels in our study, there are malities such as DV, AoI, and MPI, this
Our study of 1116 fetuses with 120 different potential sequences; we will only pick up a relatively small pro-
an EFW less than the 10th centile have, however, restricted our description portion of remaining adverse perinatal
comprised 7769 individual Doppler data of this point to 3 patterns to illustrate this outcomes.
points gathered for as long as 17 weeks concept (Figure 3, A-C).
of surveillance on some patients, with If we analyze the classic sequence C OMMENT
an average of 7.7 weeks. Five hundred (pattern 1: UA/MCA/DV), thought Despite the large amount of published
eleven patients (46%) had an abnormal to be the single most common pattern literature on ultrasound in the setting of
UA Doppler waveform in the study; of deterioration in IUGR, our data IUGR, the optimal surveillance pattern
70 patients had an UA AEDF and 8 had show that 46% (n ¼ 511) of the overall and timing of delivery remains the focus
an UA REDF. The mean time to delivery cohort developed an abnormal UA of much debate and research, with no
for patients with abnormal UA Doppler, Doppler. Eight percent (n ¼ 87) had a internationally accepted approach to
(intermittent) AEDF, and REDF was 26, sequence of an abnormal UA and MCA management.
13, and 4 days, respectively. Three hun- Doppler, and only 0.8% (n ¼ 9) in our In this large prospective cohort of
dred of the study population (27%) had cohort showed a sequential change in all IUGR pregnancies, we have demonstrated
an abnormal MCA, 133 (12%) had an 3 vessels. A similar sequence applies for multiple potential patterns of Doppler
abnormal MPI, 129 (11%) had an ab- patterns 2 (UA/DV/MCA) and 3 deterioration. The classic sequence from
normal DV, and 59 (5%) had an (MCA/UA/DV). abnormal UA to MCA to DVexists but no
abnormal AoI. To summarize these findings, Figure 4 more frequently than any of the other
The frequency of Doppler deteriora- combines various patterns of Doppler potential patterns.
tion for each vessel and the timing to deterioration. If the sequence of deteri- A major strength of this study is the
delivery is outlined in Figure 1. It is oration from UA to MCA to DV was the prospective study design. It took only
important to point out that these are most important, we would expect to 2 years to recruit 1200 pregnancies in
cumulative frequencies seen in the entire see a relatively flat line such that almost 7 centers, all of which were subjected to
study population of 1116 fetuses, and all patients with an abnormal umbilical a high degree of fetal surveillance using
given that there may or may not be a artery Doppler would next have an the most advanced Doppler techniques
significant overlap between these ab- abnormal middle cerebral artery Doppler available, which were performed by
normalities, we cannot conclude that and would next have an abnormal ductus a small group of 10 trained research

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umbilical artery AEDF to either


FIGURE 4 advanced Doppler surveillance or short-
Combination of pathways of Doppler deterioration (n [ 1116) term variation CTG surveillance. How-
ever, the randomized arm of the study
had to be discontinued after 12 months
of recruitment because of a lack of
eligible cases, despite access to a large
national obstetric population.
Of the fetal vessels studied, abnormal
UA and MCA Doppler remain the
strongest predictors of adverse outcome,
with only marginal added benefit to DV
and cardiac indices. Multivessel Doppler
may be beneficial as an adjunct assess-
ment tool in the evaluation of IUGR
to optimize timing of delivery; however,
our study questions whether a logical
sequence of deterioration in these vessels
exists, therefore making any interpreta-
tion of Doppler deterioration challenging.
A potential criticism relating to our
study design may be that there were no
prespecified delivery criteria, and there-
fore, fetuses affected by IUGR were
Figure 4 outlines the combination of sequences of Doppler deterioration demonstrating that all delivered at different time points of their
pathways show a similar pattern and that no single predominant pattern exists. disease progression, making it difficult
Unterscheider. Doppler deterioration in IUGR. Am J Obstet Gynecol 2013.
to draw conclusions from our data. It is
accepted that ours was not an interven-
sonographers. Although the study was 30 weeks). This might underestimate the tion trial but an observational study of
multicenter in nature, inconsistencies in true scope of the problem. real-world clinical practice. Given the
assessment were overcome with regular Evidence from randomized controlled large number of cases and individual
training sessions of the small cohort of trials as to whether additional Doppler Doppler measurements gathered in our
research sonographers by experienced interrogation is of benefit in optimizing study (1116 fetuses with 7769 individual
maternal fetal medicine specialists. All the timing of delivery in IUGR is lacking. Doppler data points), we believe that we
sonographers used the same ultrasound The practical challenges of performing have sufficient data to be able to make
equipment (Voluson E8; GE Healthcare, randomized trials in the setting of severe robust statements about the natural
Buckinghamshire, UK) and underwent IUGR are so difficult that they may not history of temporal Doppler changes.
regular quality assurance assessments. be able to inform clinical practice. The These data will be critically important
A possible weakness of our study re- PORTO study was initially designed as a for planning future intervention trials.
lates to the slightly late gestational age at study with both observational and ran- In the absence of evidence from such
which IUGR pregnancies were enrolled domized arms, with the aim being to randomized or intervention trials, as-
to the study (mean GA at enrollment was randomize IUGR pregnancies with sessment of fetal well-being by CTG,
biophysical profile scoring, amniotic
fluid index, UA, and MCA Doppler will
FIGURE 5
remain the standard of care. These
Doppler abnormalities capturing adverse perinatal outcome (n [ 57) findings should greatly simplify IUGR
Abnormal Abnormal Abnormal Abnormal Abnormal Abnormal Abnormal Abnormal surveillance, which may have a signifi-
UA MCA CPR DV AoI MPI UA+MCA UA+MCA+DV
cant implication for resource utilization
in contemporary obstetric practice. -
86% 51% 39% 25% 3.5% 8.8% 88% 88%
(n=49) (n=29) (n=22) (n=14) (n=2) (n=5) (n=50) (n=50)
ACKNOWLEDGMENTS
Doppler interrogation of the UA and MCA remains the most useful and practical tool in identifying
We thank Fiona Manning, the original Perinatal
fetuses at risk of adverse perinatal outcome, capturing 88% of all adverse outcomes. Ireland research manager, and the team of
CPR, cerebroplacental ratio; MCA, middle cerebral arteries; UA, umbilical arteries. Perinatal Ireland research sonographers, Fiona
Unterscheider. Doppler deterioration in IUGR. Am J Obstet Gynecol 2013. Cody, Hilda O’Keefe, Emma Doolin, Cecelia
Mulcahy, Azy Khalid, Phyl Gargan, Annette

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