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Doppler assessment of the fetus withintrauterine growth restrictionSociety for Maternal-Fetal Medicine Publications Committee, with the assistance
of Eliza Berkley, MD; Suneet P. Chauhan, MD; and Alfred Abuhamad, MD
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Intrauterine growth restriction (IUGR) isdefined as sonographic estimated fetal

weight �10th percentile for gestational age.1

AccordingtotheAmericanCollegeofObste-tricians and Gynecologists, IUGR is “one themost common and complex problems inmodern obstetrics.”2 This characterization isunderstandableconsideringthevariouspub-lished definitions, poor detection rate, lim-ited preventive or treatment options, multi-ple associated morbidities, and increasedlikelihood of perinatal mortality associatedwith IUGR. Suboptimal growth at birth islinked with impaired intellectual perfor-manceanddiseasessuchashypertensionandobesity in adulthood.2

Current challenges in the clinical manage-ment of IUGR include accurate diagnosis ofthe truly growth-restricted fetus, selection ofappropriate fetal surveillance, and optimiz-ing the timing of delivery.3-5 Despite the po-ential for a complicated course, antenataletection of IUGR and its antepartum sur-eillance can improve outcomes. The pur-ose of this document is to synthesize andssess the strength of evidence of the currentiterature regarding the use of Doppler ve-ocimetry of the umbilical artery, middle ce-ebral artery, and ductus venosus for non-nomalous fetuses with suspected IUGR,nd to provide recommendations regardingntepartum management of these pregnan-ies, inparticularforsingletongestations.Wecknowledge that defining small for gesta-

From the Society for Maternal-Fetal MedicinePublications Committee, with the assistanceof Eliza Berkley, Suneet P. Chauhan, andAlfred Abuhamad, Division of Maternal-FetalMedicine at Eastern Virginia Medical School,Norfolk, VA.

Received Jan. 11, 2012; accepted Jan. 12,2012.

The authors report no conflict of interest.

Reprints not available from the authors.

0002-9378/$36.00© 2012 Published by Mosby, Inc.

sdoi: 10.1016/j.ajog.2012.01.022

300 American Journal of Obstetrics & Gynecology

ional age (birthweight �10th percentile forestational age) by general population chartss customized charts is an important issue,ut this is not the focus of this clinicalpinion.6

Umbilical artery DopplerDoppler velocimetry of the umbilical ar-tery assesses the resistance to blood per-fusion of the fetoplacental unit (Figure 1,A). As early as 14 weeks, low impedancein the umbilical artery permits continu-ous forward flow throughout the cardiaccycle.7 Maternal or placental conditionshat obliterate small muscular arteries inhe placental tertiary stem villi result in

progressive decrease in end-diastolicow in the umbilical artery Doppleraveform until absent (Figure 1, B) and

hen reversed (Figure 1, C) flow duringiastole are evident.8 Reversed end-dia-

OBJECTIVE: We sought to provide evidencstudies for fetuses with intrauterine growthMETHODS: Relevant documents were idenMedicine, 1983 through 2011) publicationpartum outcomes of IUGR according to Docerebral artery, and ductus venosus. Addiguidelines, and studies identified throughrelevant articles. Consistent with US Prevenevaluated for quality based on the highest lgraded.RESULTS AND RECOMMENDATIONS: Sustudies indicates that, among high-risk pumbilical arterial Doppler assessment signduction, cesarean delivery, and perinatal deconfidence interval, 0.52–0.98). Antepartartery should be started when the fetus is vistudies of the ductus venous, middle cerebnostic value for IUGR fetuses, currently thereThus, Doppler studies of vessels other thanfetal well-being in pregnancies complicateprotocols.

Key words: Doppler, ductus venosus, intraartery, umbilical artery, uterine artery

tolic flow in the umbilical arterial cir-

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ulation represents an advanced stagef placental compromise and has beenssociated with obliteration of �70%f arteries in placental tertiary villi.9,10

Absent or reversed end-diastolic flowin the umbilical artery is commonly as-sociated with severe (birthweight �3rdpercentile for gestational age) IUGRand oligohydramnios.11,12

Although there are other quantitativeassessments of umbilical artery Doppler(eg, resistance index) available, the sys-tolic to diastolic (S/D) ratio and pulsatil-ity index (PI) are commonly used andeither may be sufficient to manage mostcases of suspected IUGR. When end-di-astolic flow is absent, the S/D ratio is im-measurable and PI may be used.

In clinical practice, Doppler wave-forms of the umbilical artery can be ob-

ased guidelines for utilization of Dopplertriction (IUGR).

ed using PubMed (US National Library ofritten in English, which describe the peri-r assessment of umbilical arterial, middleally, the Cochrane Library, organizationaliew of the above were utilized to identifyTask Force suggestions, references were

l of evidence, and recommendations were

ary of randomized and quasirandomizednancies with suspected IUGR, the use ofantly decreases the likelihood of labor in-s (1.2% vs 1.7%; relative risk, 0.71; 95%surveillance with Doppler of the umbilicale and IUGR is suspected. Although Dopplerartery, and other vessels have some prog-a lack of randomized trials showing benefit.umbilical artery, as part of assessment ofy IUGR, should be reserved for research

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bilical cord. Waveforms obtained nearthe placental end of the cord reflectdownstream resistance and show higherend-diastolic flow velocity than wave-forms obtained near the abdominal cordinsertion.13 To optimize reproducibility,

e suggest interrogating the umbilicalrtery at the abdominal cord insertionTable). The S/D ratio and PI should bebtained in the absence of fetal breath-

ng, and when the waveform is uniform.n clinical practice, averaging values of/D ratios or PIs is unnecessary.

Middle cerebral artery DopplerUnder normal conditions, the cerebral cir-culation is a high impedance circulationwith continuous forward flow presentthroughout the cardiac cycle14 (Figure 2,

). The middle cerebral arteries, whicharry �80% of the cerebral circulation,epresent major branches of the circle of

illis and are the most accessible cerebralessels for ultrasound imaging in the fe-us.15 The middle cerebral artery can be

imaged with color Doppler ultrasound in atransverse plane of the fetal head obtainedat the base of the skull. In this transverseplane, the proximal and distal middle cere-bral arteries are seen in their longitudinalview, with their course almost parallel tothe ultrasound beam. Middle cerebral ar-tery Doppler waveforms, obtained fromthe proximal portion of the vessel imme-diately near the circle of Willis, have shownthe best reproducibility16 (Table). A lim-ted number of studies have noted that

iddle cerebral artery peak systolic veloc-ty may be a better predictor of perinatal

ortality in preterm IUGR than the PI,ut additional study is needed to confirmhis finding.17 While angle of correction isot necessary when measuring the middleerebral artery PI, peak systolic velocityeasurement should use angle correction

nd the angle of incidence should be �30egrees; optimally as close to 0 degrees asossible.In the presence of fetal hypoxemia,

entral redistribution of blood flow re-ults in increased blood flow to the brain,eart, and adrenal glands, and a reduc-ion in flow to the peripheral circula-ions. This blood flow redistribution,
nown as the brain-sparing reflex, is
FIGURE 1Examples of umbilical artery Doppler flow waveforms

A

B

C

A, Normal umbilical artery Doppler flow waveform. B, Absent and C, reversed end-diastolic Dopplerflow in umbilical artery.SMFM. Doppler assessment of fetus with IUGR. Am J Obstet Gynecol 2012.

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characterized by increased end-diastolicflow velocity (reflected by a low PI) in themiddle cerebral artery (Figure 2, B).14,18,19

Doppler assessment of brain sparing canalso be assessed with the cerebroplacen-tal ratio, defined as middle cerebral ar-tery PI/umbilical artery PI. A fetus isconsidered to have fetal brain sparingwhen this ratio is �5th percentile forgestational age.20,21

Ductus venosus DopplerDoppler waveforms obtained from thecentral venous circulation in the fetus re-flect the physiologic status of the rightventricle. Doppler waveforms are ob-tained from the ductus venosus in atransverse or sagittal view of the fetal ab-domen at the level of the diaphragm.22

By superimposing color Doppler on thegray-scale image, the ductus venosus canbe identified as it branches from the um-bilical vein (Table). Variable high flowvelocities, reflected as a mixture of colorson color Doppler imaging (aliasing), arecommonly seen within the ductus veno-sus, and indicate an appropriate locationfor Doppler flow interrogation. Ductusvenosus Doppler waveforms are biphasicin shape with the first peak correspond-ing to ventricular systole, the secondpeak during passive filling in ventriculardiastole, followed by a nadir in late dias-tole with atrial contraction (Figure 3, A).

TABLECharacteristics of common Dopple

VariableGestationalage, wk Location

Umbilicalartery

�23 Abdominal cord inser(preferred), otherlocations acceptable

...................................................................................................................

Middlecerebralartery

�23 Proximal portion ofvessel at 0-degree aof incidence

...................................................................................................................

Ductusvenosus

�23 At site of aliasing, whit branches fromumbilical vein

...................................................................................................................

Uterineartery

18-23 As it crosses thehypogastric vessels

...................................................................................................................

AEDF, absent end-diastolic flow; IUGR, intrauterine growth resa May use gestational age–based table18 or subjective.

SMFM. Doppler assessment of fetus with IUGR. Am J Ob

Continuous forward flow throughout p


the cardiac cycle is seen in the normalfetus. Decreased, absent, or reversed flow(Figure 3, B and C) in the A wave (atrialcontraction) may represent myocardialimpairment and increased ventricularend-diastolic pressure resulting from anincrease in right ventricular afterload.This abnormal waveform in the ductusvenosus has been documented in fetuseswith IUGR and linked to an increasedneonatal mortality rate.23,24

Uterine artery DopplerDoppler velocimetry of the uterine arter-ies reveals a progressive decrease in im-pedance with advancing gestationalage.25,26 This decrease in impedance ishought to reflect a maternal adaptationo pregnancy resulting from trophoblas-ic invasion of the maternal spiral arteri-les in the first half of gestation.27 Theterine artery can be demonstrated byolor Doppler velocimetry as it origi-ates from the anterior division of theypogastric artery, and just before it en-ers the uterus at the uterine-cervicalunction. Pulsed Doppler velocimetry ofhe uterine artery should be obtained im-

ediately after the vessel crosses the hy-ogastric artery and before it divides intohe uterine and cervical branches. Thebility to obtain the uterine artery Dopp-er waveforms at all gestational ages is ap-

tudies

Pitfalls Abnormal

Optimally done when no fetalbreathing

Decreased(includes A

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�30-degree angle of incidence Increased d

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Obtaining Doppler of hypogastricartery or vaginal branch ofuterine artery

Notching opulsatility i

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on; REDF, reversed end-diastolic flow.

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roximately 95-98%.28 s

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In early gestation, a notched uterineartery Doppler waveform and low dia-stolic flow is evident due to high vascularimpedance. With advancing gestation,decreasing vascular impedance is reflectedby increased flow in diastole and in disap-pearance of the notch (Figure 4, A). Thepersistence of a uterine artery notch in thelate second and third trimesters has beenused to identify abnormal uterine circula-tion in pregnancy (Figure 4, B).23,29,30

Caution, however, should be used againstrelying solely on the presence of a notch inthe uterine artery Doppler waveform todefine an abnormal uterine circulationgiven the subjectivity involved in its iden-tification. Thus, clinicians should look alsoat the PI, with a value �95th percentile forestational age considered to be abnor-al31 (Table).

Question 1. Should Dopplerultrasound assessment be performedin low-risk and/or high-risk womenas a screening test for IUGR?(Levels II and III)Routine umbilical artery Doppler screeningfor the subsequent development of IUGR ina low-risk population has not been shown tobe effective in predicting IUGR. A meta-analysis of 4 trials (n � 11,375), which in-luded 2 studies of low-risk populations andstudiesofunselectedpopulations,foundno

Abnormality linked with

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StillbirthNeurological impairment

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tolic flowa Neonatal acidosisNeurological impairment

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Neonatal acidemiaPerinatal mortality

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ization, obstetric outcomes, or perinatalmorbidities with systematic use of umbilicalartery Doppler as compared with controlgroups.32 The metaanalysis acknowledgedhat these 4 trials had insufficient power, andhat about 30,000 women would need to beandomized to determine if routine umbili-al artery Doppler screening in a low-riskopulation would influence perinatal mor-ality.32 Thus, until additional randomized

trials are completed, Doppler screening ofthe umbilical artery should not be usedroutinely in low-risk women to predictIUGR. Among high-risk women, there areno population-based studies regarding um-bilical artery Doppler to identify pregnanciescomplicated by IUGR.

A limited number of studies have evalu-ated first-trimester uterine artery Dopplervelocimetry as a screening test for IUGR.However, the sensitivity is low (12%), pre-cluding its clinical value.33 The 2 largest

etaanalyses regarding second-trimesterterine artery Doppler screening reachediffering conclusions. Chien et al34 sum-

marized the result of 28 studies includingalmost 13,000 women and noted that thelikelihood ratio (LR) of an abnormal uter-ine artery Doppler to identify IUGR was3.6 (95% confidence interval [CI], 3.2–4.0), and that a negative result carried a LRof 0.8 (95% CI, 0.8–0.9). Cnossen et al29

identified 61 studies with �41,000 womenand noted that an increased PI with notch-ing in low-risk women had a positive LR of9.1 (95% CI, 5.0–16.7) for IUGR and a LRof 14.6 (95% CI, 7.8–26.3) for newbornbirthweight �5th percentile. In high-riskwomen, the metaanalysis by Cnossen etal29 noted that an increased RI (�0.58 or

90th percentile) in the second trimesteras associated with a positive LR of 10.9

95% CI, 10.4–11.4), and a negative LR of.20 (95% CI, 0.14–0.26) for severe IUGR.In summary, neither umbilical nor

terine artery Doppler velocimetry isecommended as a screening tool fordentifying pregnancies that will beubsequently complicated by IUGRecause of inconsistent evidence ofenefit, and because standards are

acking for the study technique, gesta-ional age at testing, and criteria for ab-
ormal test result.31 t
Question 2. What are the benefits andlimitations of Doppler studies of eachvessel when IUGR is suspected?(Levels I, II, and III)Clinicians have the options of interro-gating several vessels, with umbilical ar-tery, middle cerebral artery, and ductusvenosus being the ones most studied.

Umbilical artery Doppler evaluationof pregnancies with suspected IUGR hasbeen shown to significantly reduce in-ductions of labor (relative risk [RR],0.89; 95% CI, 0.80 – 0.99), cesarean de-liveries (RR, 0.90; 95% CI, 0.84 – 0.97),and perinatal deaths (RR, 0.71; 95%CI, 0.52– 0.98; 1.2% vs 1.7%; numberneeded to treat � 203; 95% CI, 103–4352) without increasing the rate of un-necessary interventions.2,35 Comparedo not using this type of Doppler, the usef umbilical artery Doppler studies inomen with suspected IUGR is associ-

ted therefore with maternal and perina-

FIGURE 2Examples of middle cerebral artery

A

B

A, Normal middle cerebral artery Doppler flow waow with increased diastolic flow (brain sparing)

SMFM. Doppler assessment of fetus with IUGR. Am J Obstet

al benefits. Unfortunately, published o

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tudies have not typically specified an in-ervention protocol in response to ab-ormal umbilical artery Doppler testingesults. Nonetheless, umbilical arteryoppler testing should be used inomen with suspected IUGR, and maye used to guide the timing of delivery.Middle cerebral artery Doppler veloci-etry has been found to identify a subset

f IUGR fetuses at increased risk for ce-arean delivery due to abnormal fetaleart rate patterns, and for neonatal aci-osis.21,36 Long-term follow-up of IUGR

etuses with normal umbilical arteryoppler studies but with a middle cere-ral artery PI �5th percentile revealshese infants to be at higher risk for pooreurodevelopmental outcome.37 De-pite these associations, middle cerebralrtery Doppler testing of suspectedUGR fetuses has not been evaluated inandomized trials, and no specific inter-entions have been shown to improve

oppler flow waveforms

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Doppler velocimetry of the fetal cen-tral venous circulation helps identify fe-tuses with suspected IUGR at an ad-vanced stage of compromise.5,38 Absent

r reversed flow in late diastole in theuctus venosus is associated with in-reased perinatal morbidity, fetal aci-emia, and perinatal and neonatal mor-ality.39-41 In one study of 121 IUGR

fetuses, stillbirth was only observed inpregnancies with reversed late diastolicductus venosus flow.4 Unlike umbilicalrtery and middle cerebral artery Dopp-er velocimetry, interrogation of theuctus venosus is difficult because ofmall vessel size, fetal movement, andaveform similarity to inferior vena

ava. There are no randomized trialsnvolving the use of venous Dopplertudies in the management of sus-

FIGURE 3Examples of ductus venosusDoppler flow wave forms

A

B

C

A, Normal ductus venosus Doppler flow. Abnor-mal ductus venosus Doppler waveform with B,absent and C, reversed A wave.SMFM. Doppler assessment of fetus with IUGR. Am JObstet Gynecol 2012.

ected IUGR. A trial is currently un-


erway (Trial of Umbilical and Fetallow in Europe: TRUFFLE).42

In summary, the umbilical artery is thepreferred vessel to interrogate by Dopp-ler flow velocimetry to guide manage-ment in pregnancies complicated by sus-pected IUGR, given lack of randomizedtrials using Doppler studies of othervessels.

Question 3. What is the usualprogression of Doppler abnormalitiesin suspected IUGR? Is thisprogression consistent/reliable?(Levels II and III)In the presence of hypoxemia, adaptivechanges in the fetal circulation can be de-tected by Doppler ultrasound examina-tion. These changes manifest themselvesin a variable fashion in different fetuses,but some general patterns of progressioncan be recognized. Early adaptation includespreferential shunting and distribution ofblood flow to the fetal brain, heart, and adre-nal glands at the expense of the splanchnicand peripheral circulation. This adaptivemechanism, termed “brain sparing,” is re-flected on arterial Doppler ultrasound by in-creased impedance in the umbilical arteriesand decreased impedance in the middle ce-rebral arteries. As metabolic deteriorationoccurs and the fetus loses the ability to adaptto hypoxemia, the middle cerebral arteryDoppler indices will normalize, with an evi-dent decrease in end-diastolic flow in the ce-rebral circulation.5,23,24,43,44

IUGR related to decreased placentalfunction is usually associated with in-creased umbilical artery impedance, typ-ically followed by brain sparing. Withworsening obliteration of placental ves-sels, venous shunting across the ductusvenosus occurs and results in an increasein blood volume to the heart at the ex-pense of the liver. The increase in rightventricle afterload causes further shunt-ing of blood to the left ventricle that im-proves left ventricular output. Increasedend-diastolic pressure in the right ven-tricle, combined with decreased cardiaccompliance, is reflected in a decrease, ab-sence, and ultimate reversal of bloodflow in the ductus venosus during theatrial systolic component of the wave-form. Increased reversal of flow in the
atrial systolic component of the inferior
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vena cava is also noted. Worsening pla-cental function will lead to increasedcentral venous pressure and umbilicalvenous pulsations may be seen on Dopp-ler ultrasound. These are changes thatmay be associated with an abnormal bio-physical profile and/or loss of fetal heartrate variability.

When the ductus venosus and umbil-ical venous Doppler studies become ab-normal, the risk for stillbirth increasesdramatically, compared to when only theumbilical and middle cerebral arteryDoppler studies are abnormal.45 Al-hough this is not a sufficient reason toecommend routine usage of such test-ng, it might be utilized by centers withxperience in venous Doppler. Using theombination of arterial and venousoppler testing can result in identifica-

ion of the majority of fetuses with aci-emia (sensitivity 70-90% and specific-

ty 70-80%).46,47

The sequence of arterial and venousDoppler findings is mostly limited to thepreterm idiopathic IUGR fetus and hasnot been well documented in gestationsat �34 weeks.20,36,48

In summary, in preterm IUGR fetusesthere does appear to be a natural pro-gression of changes in the Doppler ofumbilical artery, middle cerebral artery,and ductus venosus, but it has a largevariability in manifestation.

Question 4. What Doppler studyregimen should be initiated forsuspected IUGR? What otherantepartum testing may be helpfulin this setting? (Levels I, II, and III)Umbilical artery Doppler evaluation of thefetus with suspected IUGR can help differ-entiate the hypoxic growth-restricted fetusfrom the nonhypoxic small fetus, andthereby reduce perinatal mortality, andunnecessary interventions.2,8,35,49-52 Um-bilical artery Doppler studies to assess forthe presence of increased placental imped-ance and fetal cardiovascular adaptation tohypoxemia should be initiated whenIUGR is suspected and the fetus is consid-ered potentially viable. Umbilical arteryDoppler studies may help guide decisionsregarding obstetrical interventions for the
IUGR pregnancy, as shown in Figure 5.

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Since there are no randomized trialswith adequate sample size to assess theoptimal frequency of umbilical arteryDoppler assessment with IUGR, sug-gested protocols vary.53 While some ad-ocate weekly Doppler assessment, oth-rs recommend testing at 2- to 4-weekntervals.38,54 When Doppler abnormal-ties are detected in the fetal arterial cir-ulation, weekly follow-up Dopplertudies are considered usually sufficientf forward umbilical artery end-diastolicow persists.3 In the absence of specific

data regarding the optimal frequency oftesting, experts have recommendedDoppler surveillance up to 2-3 times perweek when IUGR is complicated by oli-gohydramnios, or absent or reversedumbilical artery end-diastolic flow.48

When the estimated fetal weight is�10th percentile, fetal surveillance isrecommended because of the recognizedassociation between IUGR and neonatalmorbidity and mortality, and this may beinitiated as early as 26-28 weeks.2,55 Tra-

itional surveillance of the IUGR fetusas relied on fetal heart rate testing byardiotocography or ultrasound-derivediophysical profile testing. Twiceeekly nonstress testing with weekly

mniotic fluid evaluation, or weeklyiophysical profile testing, is com-only recommended when IUGR is

uspected56,57 (Figure 5). The combi-ation of ultrasound and cardiotoco-raphic surveillance techniques haseen shown to improve outcome forUGR fetuses.58,59

Question 5. What interventions areavailable and should be consideredbased on abnormal fetal Dopplervelocimetry studies? (Levels II and III)Umbilical artery Doppler blood flowstudies can be used clinically to guideinterventions such as the frequencyand type of other fetal testing, hospi-talization, antenatal corticosteroid ad-ministration, and delivery (Figure 5).Sometimes these Doppler studies canalso help defer intervention. For exam-ple, in cases with suspected IUGR andabsent or reversed end-diastolic flow�25 weeks, aggressive obstetrical inter-ventions may be deferred until a later
gestational age given the poor prognosis
for survival and intact survival in this sit-uation. However, when the decision ismade to perform antenatal surveillanceand there is willingness to perform cesar-ean delivery for fetal indication, then an-tenatal corticosteroids should be consid-ered under this circumstance.

There are no randomized studiesthat evaluate the effect of any interven-tion based on fetal Doppler blood flow

FIGURE 4Examples of uterine artery Doppler

A

B

A, Normal and B, abnormal uterine artery DopplSMFM. Doppler assessment of fetus with IUGR. Am J Obstet

testing specific to the IUGR fetus. Once

APRIL 2012 Am

the umbilical artery Doppler flow be-comes abnormal in suspected IUGR,especially in cases of absent or reversedflow, nonstress tests, and/or biophysi-cal profiles can be performed twiceweekly, or more often. Although thereare no randomized studies to guide thedecision to hospitalize, admission maybe offered once fetal testing more oftenthan 3 times per week is deemed

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Although there is ample evidence re-garding the benefits of administration ofantenatal corticosteroids before sponta-neous preterm births, some have raisedconcern for its administration for thegrowth-restricted fetus with abnormalumbilical artery Doppler studies. In theoriginal trial by Liggins and Howie60

there was an excess of fetal deaths amongwomen with pregnancy-related hyper-tension and IUGR. The potential reasonfor the increased mortality is the tran-siently increased physiologic and meta-bolic demands associated with admin-istration of glucocorticoids. Overall,though, published evidence supports useof corticosteroids for IUGR, and closeobservation for 48-72 hours is reason-able.61 When absent or reversed umbil-ical artery end-diastolic flow is noted�34 weeks, antenatal corticosteroidsshould be administered (Figure 5).Subsequent to steroid administration,there may be transient return of end-

FIGURE 5Algorithm for clinical use of Dopplein management of suspected IUGR

Suspected IUGR

Weekly UA Dopplera

Normal UA Doppler

Consider delivery at 38-39 weeks

Decreased diastolic flow

Increase frequency of tes�ng

Consider delivery at >37 weeks

IUGR, intrauterine growth restriction; UA, uterine artery.aIn conjunction with antepartum testing.

MFM. Doppler assessment of fetus with IUGR. Am J Obstet

diastolic flow in about two thirds of the


cases, attributed to altered tone of theplacental vasculature.62

Umbilical artery Doppler can guidetiming of delivery (Figure 5). If the um-bilical artery Doppler and the antepar-tum course are reassuring, delivery ofIUGR pregnancies may be postponeduntil 38-39 weeks.2,63 For pregnanciesomplicated by IUGR with absent end-iastolic umbilical artery flow, providedther fetal surveillance has remained re-ssuring, delivery at 34 weeks should beonsidered.2,17,38 For IUGR with re-ersed end-diastolic umbilical arteryow, antenatal corticosteroid adminis-

ration followed by delivery at 32 weekshould be considered.64

RECOMMENDATIONS

Levels II and III evidence,level C recommendation1. Doppler of any vessel is not recom-

ltrasound

Abnormal UA Doppler

Absent end diastolic flow

Reversed end diastolic flow

Cor�costeroids Consider delivery at

>34 weeks

Cor�costeroidsConsider delivery at

>32 weeks

ecol 2012.

mended as a screening tool for iden-

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tifying pregnancies that will subse-quently be complicated by IUGR.

Levels I evidence,level A recommendation2. Antepartum surveillance of a viable

fetus with suspected IUGR should in-clude Doppler of the umbilical artery,as its use is associated with a signifi-cant decrease in perinatal mortality.

Levels II and III evidence,level C recommendation3. Once IUGR is suspected, umbilical

artery Doppler studies should be per-formed usually every 1-2 weeks to as-sess for deterioration; if normal, theycan be extended to less frequentintervals.

Levels II and III evidence,level C recommendation4. Doppler assessment of additional fe-

tal vessels, such as middle cerebral ar-tery and ductus venosus, has not beensufficiently evaluated in randomizedtrials to recommend its routine use inclinical practice in fetuses with sus-pected IUGR.

Level I evidence,level A recommendation5. Antenatal corticosteroids should be

administered if absent or reversedend-diastolic flow is noted �34weeks in a pregnancy with sus-pected IUGR.

Levels II and III evidence,level C recommendation6. As long as fetal surveillance remains

reassuring, women with suspectedIUGR and absent umbilical arteryend-diastolic flow may be mana-ged expectantly until delivery at 34weeks.

Levels II and III evidence,level C recommendation7. As long as fetal surveillance remains

reassuring, women with suspectedIUGR and reversed umbilical arteryend-diastolic flow may be mana-ged expectantly until delivery at 32

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This opinion was developed by thepublications committee of the Societyfor Maternal-Fetal Medicine with theassistance of Eliza Berkley, MD, SuneetP. Chauhan, MD, and Alfred Abuha-mad, MD, and was approved by the ex-ecutive committee of the society onDec. 21, 2011. Drs Berkley, Chauhan,and Abuhamad, and each member ofthe publications committee (VincenzoBerghella, MD [Chair], Sean Black-well, MD [Vice-Chair], Brenna Ander-son, MD, Suneet P. Chauhan, MD,Joshua Copel, MD, Cynthia Gyamfi,MD, Donna Johnson, MD, BrianMercer, MD, George Saade, MD, Hy-agriv Simhan, MD, Lynn Simpson,MD, Joanne Stone, MD, Alan Tita,MD, MPH, PhD, Michael Varner, MD,Deborah Gardner) have submitted aconflict of interest disclosure delin-

Quality of evidence

The quality of evidence for each includedarticle was evaluated according to thecategories outlined by the USPreventative Services taskforce:

I Properly powered and conductedrandomized controlled trial; well-conducted systematic review ormetaanalysis of homogeneousrandomized controlled trials.

.........................................................................................................

II-1 Well-designed controlled trial withoutrandomization.

.........................................................................................................

II-2 Well-designed cohort or case-controlanalytic study.

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II-3 Multiple time series with or withoutthe intervention; dramatic resultsfrom uncontrolled experiments.

.........................................................................................................

III Opinions of respected authorities,based on clinical experience; descrip-tive studies or case reports; reports ofexpert committees.

Recommendations are gradedin the following categories:

Level AThe recommendation is based on good andconsistent scientific evidence.

Level BThe recommendation is based on limited orinconsistent scientific evidence.

Level CThe recommendation is based on expertopinion or consensus.

eating personal, professional, and/

or business interests that might beperceived as a real or potential con-flict of interest in relation to thispublication. f

REFERENCES1. Battaglia FC, Lubchenko LO. A practicalclassification of newborn infants by weight andgestational age. J Pediatr 1967;71:159-63.Level II-3.2. American College of Obstetricians and Gyne-cologists. Intrauterine growth restriction; ACOGpractice bulletin no. 12. Washington, DC:ACOG; 2000. Level III.3. Baschat AA. Arterial and venous Doppler inthe diagnosis and management of early onsetfetal growth restriction. Early Hum Dev 2005;81:877-87. Level III.4. Baschat AA, Gembruch U, Reiss I, Gortner L,Weiner CP, Harman CR. Relationship betweenarterial and venous Doppler and perinatal out-come in fetal growth restriction. Ultrasound Ob-stet Gynecol 2000;16:407-13. Level II-2.5. Bilardo CM, Wolf H, Stigter RH, et al. Rela-tionship between monitoring parameters andperinatal outcome in severe, early intrauterinegrowth restriction. Ultrasound Obstet Gynecol2004;23:119-25. Level II-1.6. Gardosi J, Francis A. Adverse pregnancyoutcome and association with small for gesta-tional age birthweight by customized and pop-ulation-based percentiles. Am J Obstet Gyne-col 2009;201:28.e1-8. Level II-1.7. Fisk NM, MacLachlan N, Ellis C, Tanniran-dorn Y, Tonge HM, Rodeck CH. Absent end-diastolic flow in first trimester umbilical artery.Lancet 1988;2:1256-7. Level II-3.8. Trudinger BJ, Stevens D, Connelly A, et al.Umbilical artery flow velocity waveforms andplacental resistance: the effect of embolizationsof the umbilical circulation. Am J Obstet Gyne-col 1987;157:1443-8. Level II-3.9. Kingdom JC, Burrell SJ, Kaufmann P. Pa-thology and clinical implications of abnormalumbilical artery Doppler waveforms. UltrasoundObstet Gynecol 1997;9:271-86. Level III.10. Morrow RJ, Adamson SL, Bull SB, RitchieJW. Effect of placental embolization on the umbil-ical artery velocity waveform in fetal sheep. Am JObstet Gynecol 1989;161:1055-60. Level III.11. McIntire DD, Bloom SL, Casey BM, LevenoKJ. Birth weight in relation to morbidity andmortality among newborn infants. N Engl J Med1999;340:1234-8. Level II-2.12. Copel JA, Reed KL. Doppler ultrasound inobstetrics and gynecology, 1st ed. New York,NY: Raven Press; 1995:187–98. Level III.13. Trudinger BJ. Doppler ultrasonography andfetal well being. In: Reece EA, Hobbins JC, Ma-honey M, Petrie RH, eds. Medicine of the fetusand mother. Philadelphia, PA: JB Lipincott Co;1992. Level III.14. Mari G, Deter RL. Middle cerebral artery
flow velocity waveforms in normal and small- p
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for-gestational age fetuses. Am J ObstetGynecol 1992;166:1262-70. Level II-3.15. Veille JC, Hanson R, Tatum K. Longitudinalquantitation of middle cerebral artery blood flowin normal human fetuses. Am J Obstet Gynecol1993;169:1393-8. Level II-3.16. Mari G, Abuhamad AZ, Cosmi E, Segata M,Altaye M, Akiyama M. Middle cerebral arterypeak systolic velocity: technique and variability.J Ultrasound Med 2005;24:425-30. Level II-3.17. Mari G, Hanif F, Kruger M, Cosmi E, Santo-laya-Forgas J, Teadwell MC. Middle cerebralartery peak systolic velocity: a new Doppler pa-rameter in the assessment of growth-restrictedfetuses. Ultrasound Obstet Gynecol 2007;29:310-6. Level II-3.18. Kurmanavicius J, Florio I, Wisser J, et al.Reference resistance indices of the umbilical,fetal middle cerebral and uterine arteries at24-42 weeks of gestation. Ultrasound ObstetGynecol 1997;10:112-20. Level II-2.19. Behrman RE, Lees MH, Peterson EN, De Lan-noy CW, Seeds AE. Distribution of the circulation inthe normal and asphyxiated fetal primate. Am J Ob-stet Gynecol 1970;108:956-69. Level II-3.20. Bahado-Singh RO, Kovanci E, Jeffres A, etal. The Doppler cerebroplacental ratio and perina-tal outcome in intrauterine growth restriction.Am J Obstet Gynecol 1999;180:750-6. Level II-3.21. Cruz-Martinez R, Figueras F, Hernandez-Andrade E, Oros D, Gratacos E. Fetal brainDoppler to predict cesarean delivery for nonre-assuring fetal status in term small-for-gestation-al-age fetuses. Obstet Gynecol 2011;117:618-26. Level II-1.22. Maiz N, Kagan KO, Milovanovic Z, Celik E,Nicolaides KH. Learning curve for Doppler as-sessment of ductus venosus flow at 11 � 0 to3 � 6 weeks’ gestation. Ultrasound Obstetynecol 2008;31:503-6. Level II-2.3. Baschat AA, Hecher K. Fetal growth restric-ion due to placental disease. Semin Perinatol004;28:67-80. Level III.4. Baschat AA. Fetal responses to placental

nsufficiency: an update. BJOG 2004;111:031-41. Level III.5. Jurkovic D, Jauniaux E, Kurjak A, et al.ransvaginal color Doppler assessment of theteroplacental circulation in early pregnancy.bstet Gynecol 1991;77:365-9. Level II-3.6. Jauniaux E, Jurkovic D, Campbell S, et al.oppler ultrasonographic features of the devel-ping placental circulation; correlation with an-tomic findings. Am J Obstet Gynecol 1992;66:585-7. Level II-3.7. Papageorghiou AT, Yu CKH, Nicolaides KH.he role of uterine artery Doppler in predicting ad-erse pregnancy outcome. Best Pract Res Clin Ob-tet Gynecol 2004;18:383-96. Level III.8. Papageorghiou AT, To MS, Yu CK, Nico-

aides KH. Repeatability of measurement ofterine artery pulsatility index using transvaginalolor Doppler. Ultrasound Obstet Gynecol001;18:456-9. Level II-3.9. Cnossen J, Morris R, Riet G, et al. Use ofterine artery Doppler ultrasonography to predict
re-eclampsia and intrauterine growth restriction:


a systematic review and bivariable meta-analysis.CMAJ 2008;178:701-11. Level I.30. Campbell S, Diaz-Recasens J, Griffin DR, etal. New Doppler technique for assessing utero-placental blood flow. Lancet 1983;26:675-7.Level II-3.31. Sciscione AC, Hayes EJ. Society for Mater-nal-Fetal Medicine: uterine artery Doppler flowstudies in obstetric practice. Am J Obstet Gy-necol 2009;201:121-6. Level III.32. Goffinet F, Paris-Llado J, Nisand I, Breart G.Umbilical artery Doppler velocimetry in unse-lected and low risk pregnancies: a review ofrandomized controlled trials. Br J ObstetGynaecol 1997;104:425-30. Level I.33. Bahado-Singh RO, Jodicke C. Uterine arteryDoppler in first trimester pregnancy screening.Clin Obstet Gynecol 2010;53:879-87. Level III.34. Chien PF, Arnott N, Gordon A, Owen P,Khon K. How useful is uterine artery Dopplerflow velocimetry in the prediction of preeclamp-sia, intrauterine growth retardation and perina-tal death? An overview. BJOG 2000;107:196-208. Level I.35. Alfirevic Z, Stampalija T, Gyte GM. Fetal andumbilical Doppler ultrasound in high-risk preg-nancies. Cochrane Database Syst Rev 2010;CD007529. Level I.36. Severi FM, Bocchi C, Visentin A, et al. Uter-ine and fetal cerebral Doppler predict the out-come of third trimester small-for-gestationalage fetuses with normal umbilical artery Dopp-ler. Ultrasound Obstet Gynecol 2002;19:225-8. Level II-3.37. Eizarch E, Meler E, Iraola A, et al. Neurode-velopmental outcome in 2-year-old infants whowere small-for-gestational age term fetuses withcerebral blood flow redistribution. Ultrasound Ob-stet Gynecol 2008;32:894-9. Level II-2.38. Turan S, Turan OM, Berg C, et al. Comput-erized fetal heart rate analysis, Doppler ultra-sound and biophysical profile score in the pre-diction of acid-base status of growth restrictedfetuses. Ultrasound Obstet Gynecol 2007;30:750-6. Level II-3.39. Ozacan T, Sbracia M, d’Ancona RL, CopelJA, Mari G. Arterial and venous Doppler veloci-metry in the severely growth-restricted fetusand associations with adverse perinatal out-come. Ultrasound Obstet Gynecol 1998;12:39-44. Level II-3.40. Baschat AA, Gembruch U, Weiner CP, Har-man CR. Qualitative venous Doppler waveformanalysis improves prediction of critical perinataloutcomes in premature growth-restricted fe-tuses. Ultrasound Obstet Gynecol 2003;22:240-5. Level II-3.41. Cosmi E, Ambrosini G, D’Antona D, Sacca-rdi C, Mari G. Doppler, cardiotocography, andbiophysical profile changes in growth-restrictedfetuses. Obstet Gynecol 2005;106:1240-5.Level II-3.42. Lees C, Baumgartner H. The TRUFFLEstudy–a collaborative publicly funded project
from concept to reality: how to negotiate an

ethical, administrative and funding obstaclecourse in the European Union. UltrasoundObstet Gynecol 2005;25:105-7. Level III.43. Hecher K, Campbell S, Doyle P, HarringtonK, Nicolaides K. Assessment of fetal compro-mise by Doppler ultrasound investigation of thefetal circulation: arterial, intracardiac, and ve-nous blood flow velocity studies. Circulation1995;91:129-38. Level II-3.44. Ferrazzi E, Bozzo M, Rigano S, et al. Tempo-ral sequence of abnormal Doppler changes in theperipherals and central circulatory systems of theseverely growth-restricted fetus. Ultrasound Ob-stet Gynecol 2002;19:140-6. Level II-3.45. Baschat AA. Doppler application in the de-livery timing of preterm growth-restricted fetus:another step in the right direction. UltrasoundObstet Gynecol 2004;23:111-8. Level III.46. Baschat AA, Güclü S, Kush ML, GembruchU, Weiner CP, Harman CR. Venous Doppler inthe prediction of acid-base status of growth-restricted fetuses with elevated placental bloodflow resistance. Am J Obstet Gynecol 2004;191:277-84. Level II-3.47. Rizzo G, Capponi A, Talone PE, Arduini D,Romanini C. Doppler indices from inferior venacava and ductus venosus in predicting pH andoxygen tension in umbilical blood at cordocen-tesis in growth-retarded fetuses. UltrasoundObstet Gynecol 1996;7:401-10. Level II-2.48. Turan S, Miller J, Baschat AA. Integrated test-ing and management in fetal growth restriction.Semin Perinatol 2008;32:194-200. Level III.49. Karsdorp VH, van Vugt JM, Dekker GA, vanGeijn HP. Reappearance of end-diastolic veloc-ities in the umbilical artery following maternalvolume expansion: a preliminary study. ObstetGynecol 1992;80:679-83. Level II-2.50. Baschat AA, Weiner CP. Umbilical arteryDoppler screening for detection of the small fe-tus in need of antepartum surveillance. Am JObstet Gynecol 2000;182:154-8. Level II-2.51. Nienhuis SJ, Vles JS, Gerver WJ, HooglandHJ. Doppler ultrasonography in suspected in-trauterine growth retardation: a randomizedclinical trial. Ultrasound Obstet Gynecol 1997;9:6-13. Level I.52. McCowan LM, Harding JE, Roberts AB,Barker SE, Ford C, Stewart AW. A pilot random-ized controlled trial of two regimens of fetal sur-veillance for small-for-gestational-age fetuseswith normal results of umbilical artery Dopplervelocimetry. Am J Obstet Gynecol 2000;182:81-6. Level I.53. Grivell RM, Wong L, Bhatia V. Regimens offetal surveillance for impaired fetal growth. Co-chrane Database System Rev 2009;1:CD007113. Level I.54. Abuhamad AZ. American College of Obste-tricians and Gynecologists practice bulletin,clinical management guidelines for obstetrician-gynecologists no. 98, October 2008 (replacespractice bulletin no. 58, December 2004): ultra-sonography in pregnancy. Obstet Gynecol
2008;112:951-61. Level III.
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55. American College of Obstetricians and Gy-necologists. ACOG practice bulletin, antepar-tum fetal surveillance, no. 9, October 1999 (re-places technical bulletin no. 188, January1994): clinical management guidelines for ob-stetrician-gynecologists. Int J Gynaecol Obstet2000;68:175-85. Level III.56. Manning FA, Bondaji N, Harman CR, et al.Fetal assessment based on fetal biophysicalprofile scoring, VIII: the incidence of cerebralpalsy in tested and untested perinates. Am JObstet Gynecol 1998;178:696-706. Level II-3.57. Baschat AA, Galan HL, Bhide A, et al. Dopplerand biophysical assessment in growth restrictedfetuses: distribution of test results. UltrasoundObstet Gynecol 2006;27:41-7. Level II-2.58. Arabin B, Becker R, Mohnhaupt A, EntezamiN, Weitzel HK. Prediction of fetal distress andpoor outcome in intrauterine growth retardation–acomparison of fetal heart rate monitoring com-bines with stress tests and Doppler ultrasound.Fetal Diagn Ther 1993;8:234-40. Level II-3.59. Ott WJ, Mora G, Arias F, Sunderji S, Shel-don G. Comparison of the modified biophysicalprofile to a “new” biophysical profile incorporat-ing the middle cerebral artery to umbilical arteryvelocity flow systolic/diastolic ratio. Am J ObstetGynecol 1998;78:1346-53. Level I.60. Liggins GC, Howie RN. A controlled trial ofantepartum glucocorticoid treatment for preven-tion of the respiratory distress syndrome inprema-ture infants. Pediatrics 1972;50:515-25. Level I.61. Vidaeff AV, Blackwell SC. Potential risks andbenefits of antenatal corticosteroid therapy prior topreterm birth in pregnancies complicated by severefetal growth restriction. Obstet Gynecol Clin NorthAm 2011;38:205-14, ix. Level III.62. Robertson MC, Murila F, Tong S, et al. Pre-dicting perinatal outcome through changes inumbilical artery Doppler studies after antenatalcorticosteroids in the growth-restricted fetus.Obstet Gynecol 2009;113:636-40. Level III.63. Spong CY, Mercer BM, D’Alton M, Kilpat-rick S, Blackwell S, Saade G. Timing of indi-cated late-preterm and early-term birth. ObstetGynecol 2011;118:323-33. Level III.64. Hartung J, Kalache KD, Heyna C, et al. Out-come of 60 neonates who had ARED flow pre-natally compared with matched control groupof appropriate-for-gestational age preterm ne-onates. Ultrasound Obstet Gynecol 2005;25:566-72. Level II.

The practice of medicine continues toevolve, and individual circumstances willvary. This opinion reflects information avail-able at the time of its submission for publi-cation and is neither designed nor intendedto establish an exclusive standard of peri-natal care. This publication is not expectedto reflect the opinions of all members of the
Society for Maternal-Fetal Medicine.

doppler assessment of the fetus with intrauterine … indicates that, among high-risk pregnancies...

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