Ebook Donald school textbook of ultrasound in obstetrics and gynecology (3rd edition): Part 2

(BQ) Part 2 book Donald school textbook of ultrasound in obstetrics and gynecology presents the following contents: Doppler sonography in obstetrics, postpartum ultrasound, fetal behavior, amniocentesis and fetal blood sampling, amniocentesis and fetal blood sampling, ultrasound and uterine fibroid,...

C H A P T E R

Ultrasound in the Management

of the Alloimmunized Pregnancy

Daniel W Skupski

INTRODUCTION

Due to the advent of ultrasound imaging, the diagnosis and treatment of red blood cell (RBC) alloimmunization

is arguably the quintessential success story in obstetrics The pathophysiology is well described, the diagnosis

is easily and reliably established and life-saving treatment for the fetus and newborn is available both in

utero and after delivery with a high degree of success Ultrasound has been used for diagnosis and as an

adjunct for the treatment of RBC alloimmunization for several decades, and the applications for ultrasoundare continuing to expand This chapter will outline the current uses of ultrasound in the setting of thealloimmunized pregnancy

HISTORY

Sir Richard Liley began the modern era of fetal therapy

with the introduction of amniocentesis for testing of the

amniotic fluid for bilirubin levels by

spectrophoto-metry.1 The degree of change in the optical density at a

wavelength of 450 nm (delta OD450) of light during

spectrophotometry of amniotic fluid correlates with the

level of bilirubin in the fluid due to the preferential

absorption of light at this wavelength by bilirubin High

levels of bilirubin in amniotic fluid correlate with the

severity of RBC alloimmunization and have been used

to guide therapy Beginning around 1961, treatment for

severe RBC alloimmunization consisted of either

percutaneous intraperitoneal fetal transfusion (IPT) or

early delivery.2 At that time, imaging to guide the needle

placement for IPT was in the form of amniography

(placement of radio-opaque dye into the amniotic

cavity) followed by fluoroscopy, using radiation, to

outline the fetus and guide needle placement into the

fetal abdominal cavity Real-time ultrasound

subse-quently replaced amniography as the imaging study of

choice

Real-time ultrasound allowed the development ofpercutaneous intravascular blood transfusion to thefetus This first occurred by fetoscopy and later bycordocentesis, also known as funipuncture or per-cutaneous umbilical blood sampling (PUBS) PUBS is

an ultrasound-guided procedure.3,4 Percutaneousumbilical blood sampling allows more accuratediagnosis of fetal anemia and the need for intrauterinetherapy, by directly testing the fetal hematocrit Due toimproved imaging with ultrasound, this procedure hasbecome technically easier As a result of advances inimage quality, intrauterine transfusion (IUT) can now

be performed in the early second trimester for the rarecases that present with severe fetal anemia very early

in gestation

During the decade of the 1990s, the CollaborativeGroup for Doppler Assessment of the Blood Velocity inAnemic Fetuses studied numerous blood vessels in aneffort to find a way to reliably diagnose severe fetalanemia (that would require invasive treatment) Theywere successful with the middle cerebral artery andtheir results were published in the year 2000.5 This haspaved the way to a noninvasive method for diagnosing

CHAPTER 30 / Ultrasound in the Management of the Alloimmunized Pregnancy 493

fetal anemia, which has led to a decrease in morbidity

from invasive procedures

DIAGNOSIS

The identification of antibodies in maternal serum is

the key to finding the alloimmunized pregnancy

Ultrasound has traditionally been used after a

pregnancy is known to have RBC alloimunization in

order to identify hydrops fetalis (Figs 30.1A and B)

Severe fetal anemia can lead to hydrops fetalis and this

is probably produced by a combination of

pathophysio-logic factors, including hypoalbuminemia and hepatic

damage from extramedullary hematopoiesis.6 The fetal

hematocrit is usually below 15% when hydrops ispresent When immune hydrops fetalis is present, IUT

is lifesaving, and usually needs to be performed within1–7 days Hydrops fetalis is present when two or morefactors listed in Table 30.1 are present When only onefactor is present, this may be an early sign of hydrops,particularly in the alloimmunized pregnancy

When fetal anemia becomes severe, there can also

be changes in fetal behavior, due to the restriction ofoxygen delivery to fetal tissues The fetus may thenconserve energy by limiting its movements Thebiophysical profile is an assessment of the character andfrequency of fetal movements along with an assessment

of the volume of amniotic fluid The biophysical profilecan possibly identify the fetus who is decompensating,but may not be reliable for this purpose The biophysicalprofile does not distinguish between severe acidemia,severe anemia, advanced fetal sepsis and severe centralnervous system anomaly, nor does it determine thecause of the fetal decompensation

Ultrasound is commonly used to guide the tic procedure of cordocentesis or PUBS (Figs 30.2A toC) First, ultrasound is used to identify the umbilicalcord insertion into the placenta, then a 20 or 22 gaugeneedle is placed percutaneously through the maternalabdomen into the fetal umbilical vein at the level of theplacental cord insertion An alternative site is the fetalintrahepatic portion of the umbilical vein, which may

diagnos-be chosen if the placenta is posterior and the position

of the fetus limits accessibility to the placental cordinsertion site The placental cord insertion is generallychosen because the cord is anchored at this point,allowing the needle to easily puncture the cord.7 Freeloops of umbilical cord have rarely been used as theaccess point to the umbilical vein because their mobilitylimits the success of puncture The vein is chosenbecause it has a larger caliber and usually allows ashorter procedure time It is also thought that puncture

of an arterial vessel is more likely to produce fetalbradycardia

*Findings are listed in the order of usual progression of disease

Figures 30.1A and B: Ultrasound image of hydrops fetalis.

(A) The left image is a transverse or axial image of the fetal

chest showing bilateral large pleural effusions surrounding

the fetal heart The right image is a longitudinal or coronal

scan of the fetal thorax (towards the right of the image) and

abdomen (towards the left of the image) showing bilateral

large pleural effusions above the diaphragm; (B) Axial scan

of the fetal head in the same patient showing skin edema

(arrows)

Noninvasive Diagnosis

During the past two decades many fetal vessels andmorphologic findings have been evaluated for ultra-sound or Doppler findings that would allow a specificdiagnosis of severe fetal anemia prior to thedevelopment of hydrops fetalis An excellent review ofthis experience is available.8 The optimal time fordiagnosis of severe anemia is prior to the development

of hydrops fetalis because the mortality increases oncehydrops has occurred.9 A group of investigatorsworking consistently during the decade of the 1990s hasnow identified that the fetal middle cerebral artery peaksystolic velocity (MCA-PSV) reliably predicts fetalanemia and can be performed by sonographersconsistently with technical accuracy.5,10-13 The viscosity

of blood is inversely correlated with the speed of bloodflow in vessels Assuming the same pumping force isapplied, the lower the viscosity of blood in vessels, thehigher the velocity When fetal anemia becomes severe,the viscosity of blood is markedly decreased, and thisleads to a markedly increased peak systolic velocity.The angle of incidence at which the ultrasound beamintersects the blood flowing in a vessel affects the results

of many Doppler measurements Due to this limitation,most Doppler indices include angle correction as afeature of the software that performs the calculations.For optimal accuracy, i.e low intraobserver and inter-observer variability—the measurement of peak systolicvelocity of blood in a vessel requires that no anglecorrection be performed.10 With a 0° angle of incidence

no angle correction is needed and the measurement ofpeak systolic velocity is then very accurate

The specific technique for performing MCA-PSVmeasurements includes magnifying the image on thescreen, using color Doppler to visualize the middlecerebral artery of the fetus and adjusting the transducer

on the maternal abdomen so that the angle of incidence

of the beam to the artery is 0°, i.e the direction of bloodflow in the vessel should be aimed directly at thetransducer or directly away from the transducer(Fig 30.3) Measurements should be taken when there

is an absence of marked fetal body and breathingmovements Several measurements should be obtained

at each visit The highest MCA-PSV should be reportedand used for management decisions

The Collaborative Group for Doppler Assessment

of the Blood Velocity in Anemic Fetuses has reportedthe results of a large number of patients with fetuses atrisk for anemia who have undergone fetal MCA-PSVtesting.5,12 In their first report, they studied 110 consecu-tive pregnant women carrying 111 fetuses at risk forfetal anemia due to RBC alloimmunization evaluated

Figures 30.2A to C: Percutaneous umbilical blood sampling

or cordocentesis for intrauterine fetal transfusion.

(A) Ultrasound image of a needle being placed through the

maternal abdominal wall and placenta into the umbilical vein

at the placental cord insertion in a pregnancy with an anterior

placental attachment; (B) High resolution image of the

placental cord insertion using color Doppler; (C) High

resolution image of the needle tip in the umbilical vein (color

Doppler turned off)

CHAPTER 30 / Ultrasound in the Management of the Alloimmunized Pregnancy 495

between 15 and 36 weeks of gestation.5 They performed

MCA-PSV measurements at the time of initial referral

and every two weeks thereafter, including immediately

prior to cordocentesis Since hemoglobin concentration

in fetuses increases with gestational age, they developed

nomograms for hemoglobin concentration from 265

fetuses undergoing cordocentesis for other reasons

(suspicion of fetal infection, alloimmune

thrombo-cytopenia, immune thrombocytopenia purpura and

chromosomal anomalies) who did not have anemia The

expected values for MCA-PSV were based on

cordocentesis showed that 41 of 111 fetuses at risk for

anemia did not have anemia, 35 had mild anemia, 4

had moderate anemia and 31 had severe anemia Of

the 31 fetuses with severe anemia, 12 had hydrops

fetalis The sensitivity of MCA-PSV in detecting

moderate or severe anemia was 100% (35/35) and the

95% confidence intervals were 86–100%

Receiver-operator characteristic curves for the MCA-PSV showed

that a level of 1.5 multiples of the median (MOM) or

greater allowed a sensitivity of 100% while only

producing a false-positive rate of 12% (4/35) They

concluded that, in fetuses at risk of anemia due to RBC

alloimmunization, moderate and severe anemia can be

reliably detected by noninvasive Doppler assessment

using the middle cerebral artery peak systolic velocity

In a follow-up prospective multicenter trial with

intent-to-treat, MCA-PSV was found to be highly

predictive of moderate-to-severe anemia at delivery,

with a sensitivity of 88%, specificity of 87%, positive

predictive value of 53% and negative predictive value

of 98%.13 The diagnosis of severe anemia was missed

in one fetus, but the final outcome was good Theyconcluded that MCA-PSV will minimize fetal compli-cations associated with invasive testing in pregnanciesaffected by RBC alloimmunization and recommended

a Doppler testing within an interval of seven days.13

The same investigators also assessed the ability ofMCA-PSV in determining severe anemia longitudinally

in 34 fetuses, where measurements were performedserially They calculated the slope of the MCA-PSV ineach fetus over time and determined the average rate

of change as a function of gestational age in three groups

of fetuses: normal, mildly anemic and severely anemic.The estimated average slope increased significantly inthe severely anemic fetuses This demonstrated that theMCA-PSV can be used to follow fetuses at risk for severeanemia over the course of the pregnancy.12

The current status of MCA-PSV as a reliable methodfor the noninvasive determination of fetal anemia hasalso been confirmed by meta-analysis.14 This studyshowed that the likelihood ratio for a positive test was8.45 and for a negative test was 0.02 These results areconsistent with both clinical and statistical significance

In a prospective multicenter study, including 164women with alloimmunized pregnancies, fetal MCA-PSV measurements were demonstrated to be superior

to delta OD450 in amniotic fluid for the prediction ofsevere fetal anemia.15 These women had Rh(D), Rh(c),Rh(E) and Fy(a) antibodies, had antibody titers >1:64and antigen positive fetuses When clinical findingsnecessitated invasive assessment in this study, fetalMCA-PSV was performed first, followed by theamniocentesis Cordocentesis was performed if one orboth tests suggested severe fetal anemia (MCA-PSVabove 1.5 MOM or Liley upper zone II) Seventy-fourfetuses were diagnosed as severely anemic, defined as

a hemoglobin five standard deviations below the meanfor gestational age Fetal MCA-PSV was significantlymore sensitive than amniotic fluid delta OD 450measurements using the Liley curve (88% versus 76%,difference in sensitivity 12%, 95% CI 0.3–24.0), but wasnot more specific (82% versus 77%)

MANAGEMENT

Ultrasound has progressed from a useful adjunct to anindispensable diagnostic tool in the evaluation andtreatment of the alloimmunized pregnancy Amanagement scheme that is significantly less invasivethan previous schemes is now possible The author’s

Figure 30.3: Power and pulsed wave Doppler measurement

of the peak systolic velocity of the fetal middle cerebral artery

(MCA) The peak systolic velocity (PS) of 34.54 centimeter

per second is seen in the box in the upper right Note the

orientation of the MCA is as close to 0° as possible to that of

the ultrasound beam

algorithm for management is shown in Flow chart 30.1.

This management scheme includes the primary use of

fetal MCA-PSV measurements rather than

amniocentesis as the preferred choice for monitoring

for severe fetal anemia There are times when the fetal

MCA-PSV measurement may not be reliable and resort

to amniocentesis or cordocentesis may be necessary

Still, there are significantly fewer invasive procedures

for these women as a whole than in years past,

providing for less procedural complications and less

likelihood of iatrogenic premature delivery

Deoxyribonucleic acid (DNA) testing for the Rhesus

D (RhD) locus is a highly reliable diagnostic test and

with its use those fetuses who are truly at risk are able

to be identified DNA testing for the RhD locus allows

us to separate the fetuses who are antigen negative from

antigen positive.16 This can occur whenever fetal DNA

can be obtained at any time in gestation and is

irrespective of the paternal zygosity status The RhD

DNA testing by polymerase chain reaction (PCR) is

reliable even if paternity is unknown Fetal tissue can

be obtained by amniocentesis or chorionic villus

sampling (CVS) in early gestation and further invasiveprocedures can be avoided in those fetuses who areantigen negative and are thus not at risk for severeanemia.16 For fathers who are heterozygous for theoffending antigen, this includes 50% of fetuses.Ultrasound guidance is an essential component of thediagnostic procedures of amniocentesis and CVS.When the woman has no prior pregnancy history ofsevere fetal anemia and the fetus is antigen positive,the patient can be followed with serial ultrasound todetect hydrops fetalis and an MCA-PSV measurementperformed every one or two weeks beginning at 18weeks of gestation to detect severe fetal anemia If theMCA-PSV is greater than 1.5 MOM for the gestationalage at which it is performed, this indicates a severe fetalanemia and is an indication for cordocentesis andpossibly IUT If hydrops fetalis is identified, cordocente-sis for IUT would also be chosen

Management can be tailored based on priorpregnancy history for those fetuses that are antigenpositive Invasive testing in a subsequent pregnancybegins before the time in gestation when the fetus was

Flow chart 30.1: Management of the alloimmunized pregnancy

CHAPTER 30 / Ultrasound in the Management of the Alloimmunized Pregnancy 497

deemed to be affected in a prior pregnancy For

example, if amniocentesis showed delta OD450 in Liley

zone 3 at 28 weeks of gestation (or cordocentesis showed

severe fetal anemia) in one pregnancy, then invasive

testing would be recommended at 20–26 weeks of

gestation in the next pregnancy in previous schemes of

management Using the MCA-PSV, earlier testing

would not be required (because all patients would begin

testing at 18 weeks of gestation) unless an earlier

pregnancy was affected prior to 18 weeks An excellent

review of the current state of treatment for RBC

alloimmunization is available.17

ALLOIMMUNE THROMBOCYTOPENIA

Fetal and neonatal alloimmune thrombocytopenia is the

platelet corollary to RBC alloimmunization The natural

history of the disease shows that each subsequent

pregnancy is generally more severely affected, including

antenatal intracranial hemorrhage and fetal demise.18

Lifesaving fetal treatment is available in the form of

intravenous immune globulin (IVIG) given to the

mother on a weekly or twice weekly basis, which is

believed to act in part by limiting the placental transfer

of antiplatelet IgG antibody that attaches to fetal

platelets.19-21 Antiplatelet IgG that is transferred from

maternal plasma to the fetus is thought to coat fetal

platelets and enhance the rapid elimination of fetal

platelets by the fetal reticuloendothelial system The

ultrasound guided procedure of cordocentesis is used

to diagnose the most severely affected cases

Cordo-centesis allows fetal blood to be obtained so that a

severely low fetal platelet count can be discovered and

prenatal treatment can be instituted Review articles of

the diagnosis and treatment of alloimmune

thrombo-cytopenia are available.22,23

SUMMARY

From its beginnings as a research tool to its current

indispensable status as both a diagnostic tool and an

adjunct to therapy, ultrasound is a cornerstone in the

fight against alloimmunization Ultrasound has

advanced our knowledge of the pathophysiology and

the fetal effects of disease and our ability to manage

the alloimmunized pregnancy The Doppler MCA-PSV

measurement is a major advance in our ability to

diag-nose fetal anemia and thus manage the alloimmunized

pregnancy Advances in ultrasound imaging quality and

in our knowledge of the uses of ultrasound in the near

future should further refine our ability to diagnose and

treat the alloimmunized pregnancy

REFERENCES

1 Liley AW Liquor amnii analysis in the management of pregnancy complicated by rhesus immunization Am J Obstet Gynecol 1961;82:1359-66.

2 Liley AW Intrauterine transfusion of foetus in haemolytic disease Br Med J 1963;2(5365):1107-13.

3 Rodeck CH, Kemp JR, Holman CA, et al Direct vascular fetal blood transfusion by fetoscopy in severe thesus isoimmunization Lancet 1981;1(8221):625-7.

intra-4 Rodeck CH, Nicolaides KH, Warsof SL, et al The ment of severe rhesus isoimmunization by fetoscopic intravascular transfusions Am J Obstet Gynecol 1984; 150(6):769-74.

manage-5 Mari G, Deter RL, Carpenter RL, et al Noninvasive diagnosis by Doppler ultrasonography of fetal anemia due

to maternal red cell alloimmunization for the Collaborative Group for Doppler Assessment of the Blood Velocity in Anemic Fetuses N Engl J Med 2000;342(1):9-14.

6 Bowman JM Hemolytic disease (erythroblastosis fetalis) In: Creasy RK, Resnik R (Eds) Maternal-Fetal Medicine: Principles and Practice Philadelphia: WB Saunders Company;1994 p 719.

7 Grannum PA, Copel JA, Plaxe SC, et al In utero exchange transfusion by direct intravascular injection in severe erythroblastosis fetalis N Engl J Med 1986;314(22):1431-4.

8 Whitecar PW, Moise KJ Sonographic methods to detect fetal anemia in red blood cell alloimmunization Obstet Gynecol Survey 2000;55(4):240-50.

9 Schumacher B, Moise KJ Fetal transfusion for red blood cell alloimmunization in pregnancy Obstet Gynecol 1996;88(1):137-50.

10 Mari G, Adrignolo A, Abuhamad AZ, et al Diagnosis of fetal anemia with Doppler ultrasound in the pregnancy complicated by maternal blood group immunization Ultrasound Obstet Gynecol 1995;5(6):400-5.

11 Mari G, Rahman F, Ologsson P, et al Increase of fetal hematocrit decreases the middle cerebral artery peak systo- lic velocity in pregnancies complicated by rhesus alloimmunization J Matern Fetal Med 1997;6(4):206-8.

12 Detti L, Mari G, Akiyama M, et al Longitudinal assessment

of the middle cerebral artery peak systolic velocity in healthy fetuses and in fetuses at risk for anemia Am J Obstet Gynecol 2002;187(4):937-9.

13 Zimmerman R, Carpenter RJ, Durig P, et al Longitudinal measurement of peak systolic velocity in the fetal middle cerebral artery for monitoring pregnancies complicated by red cell alloimmunisation: a prospective multicentre trial with intention-to-treat BJOG 2002;109(7):746-52.

14 Divakaran TG, Waugh J, Clark TJ, et al Noninvasive techniques to detect fetal anemia due to red blood cell allo- immunization: a systematic review Obstet Gynecol 2001;98(3):509-17.

15 Oepkes D, Seaward PG, Vandenbussche FP, et al Doppler ultrasonography versus amniocentesis to predict fetal anemia N Engl J Med 2006;355(2):156-64.

16 Bennett PR, Le Van Kim C, Colin Y, et al Prenatal mination of fetal RhD type by DNA amplification N Engl

deter-J Med 1993;329(9):607-10.

17 Moise KJ Management of rhesus alloimmunization in

pregnancy Obstet Gynecol 2002;100(3):600-11.

18 Bussel JB, Zabusky MR, Berkowitz RL, et al Fetal

allo-immune thrombocytopenia N Engl J Med

1997;337(1):22-6.

19 Lynch L, Bussel JB, McFarland JG, et al Antenatal treatment

of alloimmune thrombocytopenia Obstet Gynecol.

1992;80(1):67-71.

20 Bussel JB, Berkowitz RL, Lynch L, et al Antenatal

management of alloimmune thrombocytopenia with

intravenous gamma-globulin: a randomized trial of the

addition of low-dose steroid to intravenous globulin Am J Obstet Gynecol 1996;174(5):1414-23.

gamma-21 Urbaniak SJ, Duncan JI, Armstrong-Fisher SS, et al Transfer

of anti-D antibodies across the isolated perfused human placental lobule and inhibition by high-dose intravenous immunoglobulin: a possible mechanism of action Br J Haematol 1997;96(1):186-93.

22 Skupski DW, Bussel JB Alloimmune thrombocytopenia Clin Obstet Gynecol 1999;42(2):335-48.

23 Bussel J Diagnosis and management of the fetus and neonate with alloimmune thrombocytopenia J Thromb Haemost 2009;7 Suppl 1:253-7.

Doppler ultrasound is a noninvasive technique whereby the movement of blood is studied by detecting thechange in frequency of reflected sound Doppler ultrasound has been used in obstetrics since 1977 to studythe fetoplacental (umbilical) circulation,2 and since the 1980s to study the uteroplacental (uterine) circulation3

and fetal circulation.4 Recently, this method became an important tool for qualifying pregnancies in risk.Information obtained with Doppler sonography helps obstetricians managing patients in situations likepregnancies complicated by intrauterine growth restriction (IUGR), Rhesus alloimmunization, multiplepregnancies and anamnestic risk factors Examination of the uteroplacental and fetomaternal circulation byDoppler sonography in the early second trimester helps predicting pregnancy complications like preeclampsia,IUGR and perinatal death.5-13

This chapter aims to introduce Doppler sonographic examinations in modern obstetrics Doppler blood flowvelocity waveforms (FVWs) of the fetal arterial side (umbilical arteries, descending aorta and middle cerebralarteries) and maternal side (uterine arteries) are discussed and nomograms for routine obstetric practice arepresented

THE SAFETY OF DOPPLER ULTRASOUND IN

OBSTETRICS

The data available suggests that diagnostic ultrasound

has no adverse effects on embryogenesis or fetal growth

In addition, ultrasonographic scanning has no long-term

effects on cognitive function or change visual or hearing

functions According to the available clinical trials, there

is a weak association between exposure to

ultrasono-graphy and non-right handedness in boys (odds ratio

1.26; 95% CI, 1.03–1.54).14 However, although B and M

mode scans are safe during pregnancy, color, power

and pulsed Doppler procedures should be performedwith caution, especially in the early stages of pregnancy,due to possible thermal effects Studies concerned withthe safety of ultrasound included mostly exposuresbefore 1995, when the acoustic potency of the equipmentused was lower than in modern machines Over theyears, there has been a continuous trend of increasingacoustic output, and the findings of the previous studiesnecessarily apply to currently used equipment Because

of weak regulation of ultrasound equipment output,fetal exposure using current equipment can be almosteight times greater than that used previously, regardless

of whether gray-scale imaging, the three-dimensional

technique, color Doppler or duplex Doppler is

employed A short acquisition time of any kind of

diagnostic ultrasonic wave may decrease exposure and

thus unknown effects on fetal development.15

In particular, the use of pulsed Doppler involves the

use of higher intensities compared to diagnostic

ultra-sound, and hence may cause significant tissue heating

and thermal effects However, these thermal effects

depend on the presence of a tissue/air interface and

may therefore not be clinically significant in obstetric

ultrasound examinations.16 The principle known as

ALARA (as low as reasonably achievable) is generally

supported and encourages the balance between the

necessary medical information, minimal settings and

exam time.17

In a randomized controlled prospective study,

considering the long-term effect of ultrasound

examinations on childhood outcome up to 8 years of

age, it was shown that exposure to multiple prenatal

ultrasound examinations from 18 weeks’ gestation

onwards might be associated with a small effect on fetal

growth, but is followed in childhood by growth and

measures of developmental outcome similar to those in

children who had received a single prenatal scan.18

DEPENDENCY OF DOPPLER FLOW VELOCITY

WAVEFORMS ON GESTATIONAL AGE

The amount of perfusion in trophoblastic tissue is

related to gestational age For this reason, in interpreting

the Doppler sonographic findings, gestational age must

be taken into account That is, nomograms for Doppler

sonographic measurements should be standardized

according to gestational age In the routine use of

ultrasound in practice, the accepted time for starting

Doppler sonographic examinations is the beginning of

the second trimester This is the right time that allows

modifications in antenatal care in a high risk pregnancy

For specific conditions, earlier timing of measurements

may be considered.19

The main objective in constituting fetomaternal

Doppler sonographic nomograms is to improve

peri-natal outcome in high risk pregnancies Curves

presen-ted below depict normal fetal and maternal Doppler

sonographic values, and can be used in routine practice

Indices

Blood flow velocity in the fetal circulating system

depends on the type of vessel: The arteries always have

a pulsatile pattern, whereas veins have either a pulsatile

or continuous pattern

Analysis of Doppler sonographic FVWs tively, is more difficult than analyzing qualitatively.Qualitative analysis also overcomes erroneous measure-ments in small vessels There are plenty of indices forqualitative analysis

quantita-Following are the most frequently used indices:

• Systolic/Diastolic ratio (S/D ratio, Stuart 1980)

• Resistance index (RI, Pourcelot 1974)

• Pulsatility index (PI, Gosling and King 1977)

In analyzing sonographic results and calculatingindices, following characters are used:

S = Temporal peak of maximum frequency

D = End-diastolic maximum frequency

C = Temporal average of maximum frequency, Fmean

I = Instantaneous spatial average frequency

E = Temporal average of spatial average frequencyCalculations of formulas are as follows (Fig 31.1):S/D ratio = S/D

RI = (S–D)/S

PI = (S–D)/CWhile calculating PI values, in some sonographicdevices, E values are used instead of C values As aresult PI values increase slightly

The above presented indices overcome also a veryserious problem involved with the angle between theultrasound beam and the direction of blood flow(insonation angle) These indices are relatively angleindependent and are therefore easily applied in clinicalpractice

In practice, none of the indices is superior to theother20-22 and any index may be used Although theS/D ratio is easily calculated, RI is the easiest to inter-pret Resistance index values approach to zero if theresistance decreases and approach to one if resistanceincreases If end-diastolic flow is absent, PI is the onlyindex making evaluation of blood flow possible, because

Figure 31.1: Scheme of the Doppler curve (I) S= systolic,

D= diastolic, C= temporal average of maximum frequency Calculation formulas of the main Doppler sonographic indices (II)

CHAPTER 31 / Doppler Sonography in Obstetrics 501

in this situation S/D will equal to infinite and RI to

one The PI is more complex because it requires the

calculation of the mean velocity, but modern Doppler

sonographic devices provide those values in real time

Doppler sonographic nomograms are used for the

differentiation of normal and abnormal blood FVWs,

which helps to determine pregnancies at risk By taking

threshold values of pathologic pregnancies into

consideration, nomograms are capable to differentiate

between normal and abnormal The nomograms are

presented for meeting this target.23 While confronting

with these nomograms, it must always kept in mind

that the values on these nomograms should not be taken

as mathematical equations, and that limitations of

sensitivity and specificity exist

Using Nomograms in Practice

Just like the defense mechanism of peripheral

vasocons-triction in an adult in the face of hemorrhagic shock,

the “brain sparing” mechanism (brain-sparing effect)

becomes active in a fetus with hypoxia or chronic

placental insufficiency As a result of the brain sparing

effect, resistance either in the umbilical artery (UA) and

fetal descending aorta (FDA) increases As a

conse-quence Doppler indices related to these vessels increase

The end-diastolic blood flow increases in middle

cerebral arteries (MCA) by the same effect Doppler

indices for this vessel decreases consequently

Some points should be considered while using

Doppler sonographic nomograms:

• Among the measurements performed on the UA and

FDA, values between 90–95th percentiles should be

considered as borderline and repeat follow-ups

should be planned Values exceeding the 95th

percentile are considered abnormal

• Doppler values between 5–10th percentiles in MCA

should be considered as borderline and repeat

follow-ups should be planned Values below the 5th

percentile are considered abnormal

• Measurements taken after 24 weeks’ gestation from

uterine arteries are more valuable The early diastolic

notching, and values exceeding the 95th percentile

are considered as abnormal One point to remember

is that notching predicts an increased risk of

preeclampsia

CHANGES IN DOPPLER SONOGRAPHIC

RESULTS DURING THE COURSE OF

PREGNANCY AND COMPLICATED

PREGNANCIES

During the course of pregnancy and in some

specific pregnancy complications, Doppler

sono-graphic results of fetomaternal vessels displaychanging values

Umbilical Artery (UA)

It has been shown in a longitudinal observational studythat Doppler ultrasound of the UA is more helpful thanother tests of fetal wellbeing (e.g heart rate variabilityand biophysical profile score) in distinguishing betweenthe normal small fetus and the “sick” small fetus.24

However, its exact role in optimizing management,particularly timing of delivery, remains unclear, and iscurrently being investigated by many study groups Theoptimal timing of delivery in pregnancies complicated

by highly pathological Doppler flow findings is still anissue to be resolved To resolve this question and toimprove the perinatal morbidity and mortality somemulticenter clinical trials25 have been undertaken.Gestational age, Doppler waveforms, antenatal testing,and maternal status should all be taken into consi-deration to guide optimal timing of delivery to minimizeextreme prematurity, but also to prevent intrauterineinjury, in the case of the compromised fetus

Blood flow velocity in the UA increases with theadvancing gestation As a result impedance to bloodflow continuously decreases due to increasing arterialblood flow in the systole and diastole End-diastolicvelocity is often absent in the first trimester2,26 and thediastolic component increases with advancinggestation27 (Fig 31.2) With advancing gestational age,end-diastolic flow becomes evident during the wholeheart cycle (Fig 31.3), proven with previous longitudi-nal studies of Fogarty et al22 and Hünecke et al,28 aswith many cross-sectional studies.27,29

Figure 31.2: Absent end-diastolic flow of the umbilical artery

in the first trimester (physiologic) with pulsations of the umbilical vein (physiologic)

Trudinger et al.30 explained this phenomenon with

the following mechanisms:

• Continuous maturation in placental villi

• Continuous widening of placental vessels cause a

continuous decrease in vascular resistance

• Continuous increase in fetal cardiac output

• Continuous changes in the vessel compliance

• Continuous increase in fetal blood pressure

Especially in the third trimester of pregnancy,

depending on the above factors normal values become

scattered on nomograms (Fig 31.4) This scattering is

more prominent in the S/D ratio than the PI Resistance

index is not affected by above factors after 28 weeks’

gestation (Figs 31.4 to 31.6)

Flow velocity waveforms of the UA are slightly

different at the abdominal wall and the placental site,

with indices higher at the fetal abdominal wall than the

placental insertion.31 The difference, however, is

minimal, and therefore in clinical practice it is notimportant to obtain the FVWs always at the same level.Flow velocity waveforms must always be obtainedduring fetal apnea periods because fetal breathingaffects the waveforms

In case of an abnormal test, clinical experience andrandomized controlled trials showed significantassociation with an adverse perinatal outcome

Intrauterine Growth Restriction

The IUGR fetus is a fetus that does not reach its potentialgrowth Environmental factors responsible for IUGRmay be due to maternal, uteroplacental and fetal factors(Table 31.1) Many authors have reported on theassociation between an abnormal UA Doppler FVW andIUGR

Differentiating the fetus with pathologic growthrestriction that is at risk for perinatal complications fromthe constitutionally small but healthy fetus has been anongoing challenge in obstetrics Not all infants whose

Figure 31.3: Normal flow velocity waveforms of the

umbilical artery in the third trimester

Figure 31.4: Umbilical artery systolic/diastolic (S/D)

ratio nomogram

Figure 31.5: Umbilical artery resistance index (RI) nomogram

Figure 31.6: Umbilical artery pulsatility index (PI) nomogram

CHAPTER 31 / Doppler Sonography in Obstetrics 503

birth weight is below the 10th percentile have been

exposed to a pathologic process in utero; in fact, most

small newborns are constitutionally small and healthy

Doppler sonography has become the most important

investigation method to differentiate between these

fetuses

Pathophysiology of abnormal FVWs in placental

insuffi-ciency:32 In the presence of placental insufficiency, there

is greater placental resistance, which is reflected in a

decreased end-diastolic component of the UA

FVWs.33-37 An abnormal UA FVW has a S/D ratio above

the normal range As the placental insufficiency

worsens, the end-diastolic velocity decreases (Fig 31.7),

then become absent (Fig 31.8) and finally it is reversed

(Fig 31.9) Some fetuses have decreased end-diastolic

velocity that remains constant with advancing gestation

and never become absent or reversed, which may be

due to a milder form of placental insufficiency Pitfalls

can be caused due to a high selected wall filter or fetal

breathing (Fig 31.10)

Abnormal UA Doppler studies, but not normal

results were found to be associated with lower arterial

and venous pH values, an increased likelihood of

intrapartum fetal distress, more admissions to the

Figure 31.7: Abnormal flow velocity waveforms of the

umbilical artery in the third trimester (high resistance index)

Figure 31.8: Absent end-diastolic flow (AEDF) of the

umbilical artery in the third trimester

Figure 31.9: Reverse flow (RF) of the umbilical artery

neonatal intensive care unit (NICU), and a higher

incidence of respiratory distress in IUGR fetuses.38

Therefore, intensive antenatal surveillance in fetuses

with suspected IUGR with a normal UA Doppler FVW

was not recommended by the authors Conflicting data

were presented by McCowan et al;39 they confirmed that

abnormal UA Doppler studies are associated with a

poor perinatal outcome in IUGR fetuses but also

concluded that the perinatal outcome in small for

gestational age fetuses with normal UA Doppler studies

is not always benign (i.e low ponderal index, postnatal

hypoglycemia, admission to the NICU) Recently, our

study group40 suggested that reversed flow should be

seen as a particular clinical entity with the higher

incidences of severe IUGR, perinatal and overall

mortality compared to absent end diastolic flow

(Figs 31.8 and 31.9)

In our clinical experience, when an IUGR fetus is

suspected, the UA, FDA and MCA are the first fetal

vessels to be assessed The ductus venosus (DV),

umbilical vein, inferior vena cava Doppler examinations

are secondary vessels to be examined, only when an

abnormal FVW is detected on the arterial vessels

Adding serial Doppler evaluation of the UA, MCA and

DV to IUGR surveillance will enhance the performance

of the biophysical score in the detection of fetal

compromise and therefore optimizing the timing of

intervention.41

Chromosomal Abnormalities

It was shown that absent end-diastolic flow in the UA

is associated with chromosomal abnormalities like

trisomies, triploidies or chromosomal deletions.42

Setting out from the point that structural anomalies aremore frequent in fetuses with chromosomal aberrations,

a rapid acquisition of a karyotype in fetuses withcongenital anomalies and an absent end-diastolic flow

in the UA is recommended.43

Impact on Perinatal Consequences

Abnormal UA FVWs are associated in IUGR fetuseswith one of the following outcomes: early delivery,reduced birth weight, oligohydramnios, NICUadmission, and prolonged hospital stay.32,44 In a meta-analysis, it was shown that the use of UA Dopplersonography in pregnancies complicated by IUGRreduces perinatal mortality up to 38% and improvesperinatal outcome.45 A review consisting of 7,000 high-risk pregnancies46 found that Doppler ultrasound wasassociated with a trend toward reduction in perinataldeath especially in pregnancies complicated withpreeclampsia or IUGR The Doppler ultrasound use wasalso associated with fewer inductions of labor and fewerhospital admissions, without reports of adverseperinatal effects The reviewers concluded that the use

of Doppler ultrasound in high-risk pregnancies is likely

to reduce perinatal mortality

Neonatal Intraventricular Hemorrhage

Fetal status as well as neonatal complications ofprematurity in IUGR both contribute to adverseperinatal outcome and increase the risk for thedevelopment of intraventricular hemorrhage (IVH).Data suggest that absent and reversed end-diastolic flow

in the UA early in gestation carries a high risk ofsubsequent neonatal IVH.47 However, this observation

is not independent of other perinatal variables:prematurity and difficult births remain the mostimportant determinants of this complication

Neuromotoric Outcome

Valcomonico et al.44 evaluated the association of UADoppler velocimetry with long-term neuromotoricoutcome in IUGR fetuses with normal (n=17), reduced(n=23) and absent or reversed (n=31) UA end-diastolicflow The infants who survived the neonatal period wereobserved for a mean of 18 months Their postural,sensorial and cognitive functions were evaluated at 3,

6, 9, 12 and 18 months of age Although, due to smallnumber of cases, the results did not reach statisticalsignificance, the incidence of permanent neurologicalsequelae increased as the UA end-diastolic flowdecreased (35% with absent or reversed flow, 12% withreduced flow, and 0% with normal flow) Recently, in

Figure 31.10: Pitfalls in umbilical artery Doppler

velocimetry (fetal breathing)

CHAPTER 31 / Doppler Sonography in Obstetrics 505

another study48 23 IUGR fetuses with absent or reversed

UA end-diastolic flow were matched with fetuses with

appropriate growth All children were followed for 6

years and intellectual and neuromotor development was

significantly diminished in fetuses with abnormal

FVWs Only social development was not impaired in

fetuses with abnormal UA FVWs Similar results were

previously published by our working group, too.49,50

Intrapartum Studies

A review of intrapartum UA Doppler velocimetry for

adverse perinatal outcome gave disappointing results.51

Out of 2,700 pregnancies, which were evaluated for the

intrapartum use of Doppler velocimetry showed that it

is a poor predictor for measures like low Apgar scores,

intrapartum fetal heart rate abnormalities, umbilical

arterial acidosis and cesarean section for fetal distress

Umbilical Artery Doppler Ultrasound in

Unselected Patients

Theoretically, the use of routine UA Doppler ultrasound

in unselected or low risk pregnancies would be to detect

those pregnancies in which there has been failure to

establish or maintain the normal low-resistance

umbilical and uterine circulations (a pathological

process leading to placental dysfunction and associated

with intrauterine growth retardation and preeclampsia),

before there is clinical evidence of fetal compromise In

practice, observational and longitudinal studies of

Doppler ultrasound in unselected or low-risk

pregnan-cies have raised doubts about its application as a routine

screening test, and authors have cautioned against its

introduction into obstetric practice without supportive

evidence from randomized trials.52-54 The relatively low

incidence of significant, poor perinatal outcomes in low

risk and unselected populations presents a challenge in

evaluating the clinical effectiveness of routine UA

Doppler ultrasound, as large numbers are required to

test the hypothesis

Multiple Gestation

The S/D ratio of twins at the UA are in agreement with

singleton pregnancies in the third trimester.55 Twins

with an abnormal UA FVW tend to be born earlier, have

a higher perinatal mortality and morbidity, and have

more frequent structural anomalies than fetuses without

abnormal Doppler results.56

Discordant growth between the twins may occur in

the cases of twin-twin transfusion syndrome, a poor

placental implantation site or chromosomal anomalies

Discordant growth is a very high-risk situation, with a

high perinatal mortality and morbidity The diagnosis

is made mainly by ultrasound biometry The bestpredictor for the diagnosis of discordant twins appears

to be the presence either a difference in the UA S/Dratio greater than 15% or a different estimated fetalweight greater than 15%.57 Recently it has been reportedthat abnormal UA FVW can be observed in small twinsmore often in monochorionic than dichorionic twins.58

Doppler ultrasound abnormalities of the UA in eithertwin are associated with poor perinatal outcome in twin-twin transfusion syndrome

The Biophysical Profile and Multivessel Doppler Ultrasound in IUGR

Biophysical profile scoring (BPS) and Doppler lance are the primary methods for fetal assessment inIUGR As placental insufficiency worsens, the fetusadapts by progressive compensation Previously, it hasbeen suggested that the sequential changes in arterialand venous flow occur before some biophysicalparameters (fetal tonus, movement, breathing, amnioticfluid volume and nonstress test)) decline.59,60 Baschat

surveil-et al.41 evaluated whether multivessel Doppler meters (UA, UV, MCA, DV and inferior vena cava)precede biophysical fetal parameters in fetuses withsevere IUGR They found that combining multivesselDoppler and composite BPS will provide significantearly warning and a definitive indication for action inthe management of severe IUGR, and suggested thatdelivery timing may be based on this new standard Inthe preterm growth-restricted fetus, timing of deliveryshould be critically determined by the balance of fetalversus neonatal risks.61

para-Fetal Descending Aorta (FDA)

Beside the UA, routine Doppler sonographicexamination at the descending fetal aorta is possible.Flow velocity waveforms of the FDA are usuallyrecorded at the level of the diaphragm Infact, FVWs atthe level of the diaphragm and distally to the origin ofthe renal arteries are different.62 Normal blood FVWs

in the FDA is highly pulsatile, with a minimal diastoliccomponent (Fig 31.11) The descending part of the aortaprovides perfusion to the fetal abdominal organs,umbilical-placental circulation and lower extremities.The FVW of the FDA shows a continuous forwardstream during the whole heart cycle, but whencompared to the FVW of the UA, the end-diastolic flow

is less than the systolic component Due to this reasonthe S/D ratio in the fetal aorta goes far than the S/D

ratio in the UA As pregnancy advances, the fetal aortic

diameter gets wider, which decreases peripheral

resistance and increases diastolic flow component

Nevertheless, this does not cause a significant S/D ratio

decrease in the FDA.63 Resistance and pulsatility indices

in the last trimester are also not affected significantly,

and show a similar course as in the UA

Increased placental impedance combined with

redistribution of blood flow from nonvital to vital

organs may result in changes in the aortic FVWs An

elevated S/D ratio, RI and PI (Figs 31.12 to 31.15) is

associated with both IUGR and adverse perinatal

outcomes, such as severe growth restriction, necrotizing

enterocolitis, fetal distress and perinatal mortality.64-71

Absent end-diastolic flow at the FDA is also a predictor

of fetal heart rate abnormalities (Fig 31.16) It wasshown that absent flow in the FDA were detected 8 days

Figure 31.11: Normal flow velocity waveforms of the fetal

descending aorta in the third trimester

Figure 31.12: Abnormal flow velocity waveforms of the fetal

descending aorta in the third trimester (high resistance index)

Figure 31.13: Descending fetal aorta S/D ratio nomogram

Figure 31.14: Descending fetal aorta RI nomogram

Figure 31.15: Descending fetal aorta PI nomogram

CHAPTER 31 / Doppler Sonography in Obstetrics 507

prior to the onset of decelerations at fetal heart rate

monitoring.68 The sensitivity and specificity of absent

end-diastolic flow in the FDA for prediction of IUGR

with fetal heart rate abnormalities are 85% and 80%,

respectively.70,71

Abnormal FVWs of the FDA were also evaluated

for intellectual function, and minor neurological

dysfunction.49,50,72,73 At 7 years of age, verbal and global

performances as well as neurological examination were

significantly better in the fetuses with normal aortic

FVWs The association found between abnormal fetal

aortic velocity waveforms and adverse outcome in terms

of minor neurological dysfunction suggests that

hemodynamic evaluation of the fetus has a predictive

value regarding postnatal neurological development.72

Albeit, most of the studies showed Doppler

veloci-metry abnormalities of the FDA is a predictive test for

the onset of decomposition due to placental ciency in the IUGR fetuses (Figs 31.16 and 31.17), itcannot be recommended as a screening or diagnostictest for IUGR in an unselected obstetric population.74

insuffi-Middle Cerebral Artery (MCA)

The circle of Willis is composed anteriorly of the anteriorcerebral arteries (branches of the internal carotid arterythat are interconnected by the anterior communicatingartery) and posteriorly of the two posterior cerebralarteries (Branches of the basilar artery that areinterconnected on either side with internal carotid artery

by the posterior communicating artery).75 These twotrunks and the MCA, another branch of the internalcarotid artery, supply the hemispheres on each side(Fig 31.18) All of the defined arteries have differentFVWs, therefore, it is important to know which artery

is being examined during clinical practice.76

The most favorably positioned vessel for Dopplersonographic examination of fetal brain perfusion is theMCA As the pregnancy advances, the vascularresistance in the MCA decreases (Fig 31.19) and theDoppler indices change (Figs 31.20 to 31.22).77 Duringthe early stages of pregnancy, end-diastolic flowvelocities in cerebral vessels are small or absent, butvelocities increase towards the end of gestation In thenormal developing fetus, the brain is an area of lowvascular impedance and receives continuous forwardflow throughout the cardiac cycle Intrauterine growthrestriction due to placental insufficiency is likely to becaused by redistribution of fetal blood flow in favor ofthe fetal brain and “stress organs”, at the expense ofless essential organs such as subcutaneous tissue,kidneys and liver Finally, the already low resistance toblood flow in the brain drops further to enhance brain

Figure 31.16: Absent end-diastolic flow (AEDF) of the

fetal descending aorta (FDA) in the third trimester

Figure 31.17: Reverse flow (RF) in

the fetal descending aorta

Figure 31.18: Circle of Willis and middle cerebral artery

visualized with color Doppler

circulation (Fig 31.23) This results with increased diastolic velocities, and a decrease in the S/D ratio ofthe MCA (Brain sparing effect).78

end-Abnormalities of the UA flow correlated with fetalcompromise better than intracerebral artery blood flowimpairment This suggests that high placentalimpedance precedes the onset of the “brain sparingeffect” In a study, in which 576 high risk pregnancieswere evaluated for the UA and MCA velocimetry,neither test was able to predict adverse perinataloutcome in the normal growing fetus.79 Results showedthat simultaneous assessment of UA and MCAvelocimetry in IUGR fetuses did not improve theperinatal outcome When the UA velocimetry wasnormal, the MCA velocimetry did not improve theprediction of IUGR or adverse perinatal outcome

Figure 31.19: Normal flow velocity waveforms of the

middle cerebral artery in the third trimester

Figure 31.20: Middle cerebral artery S/D ratio nomogram

Figure 31.21: Middle cerebral artery RI nomogram

Figure 31.22: Middle cerebral artery PI nomogram

Figure 31.23: Abnormal flow velocity waveforms of the middle

cerebral artery in the third trimester (brain sparing effect)

CHAPTER 31 / Doppler Sonography in Obstetrics 509

However, when both arteries velocimetric values were

abnormal, the risk of being growth restricted and having

an adverse perinatal outcome was doubled

It has been reported that the MCA PI is below the

normal range when pO2 is reduced.80 Maximum

reduc-tion in PI is reached when the fetal pO2 is 2–4 standard

deviations below normal for gestation When the oxygen

deficit becomes greater, there is a tendency for the MCA

PI to rise; this presumably reflects the pre-final stage

due to development of brain edema (Fig 31.24)

Hyperactivity of fetus, increase of intrauterine

pressure (e.g polyhydramnios), and external pressure

to the fetal head (e.g by the probe) might erroneously

increase end-diastolic flow velocities in the MCA.81

Different investigators have undertaken studies —

utilizing data obtained from the UA and MC—to

develop indices for evaluation of intrauterine risk.75

Prediction of Fetal Hemoglobin in Red Cell

Alloimmunization

Fetal anemia caused by red cell alloimmunization can

be detected noninvasively by Doppler ultrasound on

the basis of an increase in the peak systolic velocity in

the MCA.82,83 Although there is not a strong correlation

between these two parameters when the fetus is

nonanemic, the correlation becomes stronger as the

hemoglobin levels decrease.83 Prospective evaluation of

the MCA peak systolic velocity to detect fetuses at risk

for anemia in red cell alloimmunization showed that

90 of the 125 anticipated invasive procedures could be

avoided.84

In anemic fetuses, changes in hematocrit lead to a

corresponding alteration in blood viscosity and to an

impaired release of oxygen to the tissues Increasedcardiac output and vasodilatation are the mainmechanisms by which the fetus attempts to maintainthe oxygen and metabolic equilibrium in various organs

It is likely that when the fetus is nonanemic or mildlyanemic, there are only minor or insignificant hemo-dynamic changes Therefore, the blood velocity does notchange When the fetus becomes more anemic, variousmechanisms compensate to maintain the oxygen andmetabolic equilibrium in the various organs The MCApeak systolic velocity changes proportionally to thehemoglobin deficiency

Doppler measurements appear to be valuable forestimating hemoglobin concentration in fetuses at riskfor anemia Doppler sonography of the MCA has thepotential to decrease the need for invasive testing(amniocentesis, cordocentesis) and its potential risks.85,86

FETAL VENOUS CIRCULATION

In recent years research on the fetomaternal circulationhas focused more on the venous side of the fetalcirculation Physiologically, blood flow velocities in theumbilical vein (UV) and the portal circulation are steadyand non-pulsatile However, it has been shown that bothfetal body and breathing movements can interrupt thesevenous FVWs In a recent review, it was concluded thatseveral pathologic conditions such as nonimmunehydrops, severe IUGR, and cardiac arrhythmias alsoresult in an abnormal, pulsatile venous blood flow.87

However, the relationship between fetal venous bloodflow patterns and imminent fetal asphyxia or fetal death

is still unknown Many studies on venous circulation

in the fetal brain88 and pulmonary venous circulation

in the diagnosis of pulmonary hypoplasia wereperformed.89 Recent findings promote the use of venousDoppler to aid in timing delivery of severely growth-restricted fetuses Whereas initially it appeared thatabnormalities in ductus venosus waveform were theendpoint for pregnancies afflicted with intrauterinegrowth restriction, newer data suggest that these abnor-malities may plateau prior to further fetal deterioration

as witnessed by changes in the biophysical profile.90

Umbilical Vein (UV)

Oxygenated blood returning from the placenta runsfrom the UV through DV and inferior vena cava.Approximately 20–30% of the blood in the UV goesthrough the DV and the remaining well oxygenatedblood perfused the left lobe of the liver91 (Figs 31.25 to31.27) Normally after 15 weeks’ gestation the umbilical

Figure 31.24: Absent end-diastolic flow after the brain sparing

effect (de-centralization) this presumably reflects the prefinal

stage due to development of brain edema

vein has continuous forward blood flow.90 The presence

of UV FVW pulsatility has been associated withincreased perinatal morbidity and mortality.92,93 In ananimal model, Reed et al evaluated the UV Dopplerflow patterns and concluded that pulsations of the UVvelocity reflect atrial pressure changes that aretransmitted in a retrograde fashion.94 In some studies,

it was also observed that UV pulsations are detected infetuses with abnormal UA FVWs and/or fetal heart rateabnormalities.93 More recently, Ferrazzi et al.95 showedthat UV blood flow is reduced in IUGR fetuses andsuggested that long-term studies be performed toevaluate the clinical implications of their finding.Umbilical vein pulsations were also reported inpregnancies with nonimmune hydrops fetalis.96 In thisstudy, all the fetuses without venous pulsationssurvived, but only 4 of the 14 fetuses with pulsationssurvived Fetuses with pulsation in the UV in lategestation have a higher morbidity and mortality, even

in the setting of normal UA blood flow.97 When UVpulsations are found in an IUGR fetus, it is oftenaccompanied by reversal of the umbilical artery end-diastolic flow and reversal of the atrial “kick” on ductusvenosus waveform, which is an ominous sign.90

Inferior Vena Cava

The flow profile within this vessel is complex: it consists

of two phases of forward flow (Systolic and earlydiastolic), followed by a component of reversed flow inlate diastole87 (Figs 31.28 and 31.29) Like other venousflow patterns, the FVWs are affected by fetal body andbreathing movements The FVW can be used fordiagnosis of fetal arrhythmias, by comparing it with theFVW of the fetal aorta due to its proximity.98 In IUGRfetuses, the FVW is characterized by an increasedreversed flow during atrial contraction.99 The mecha-

Figure 31.25: Normal flow in the umbilical vein

in the third trimester (without pulsations)

Figure 31.26: Abnormal flow in the umbilical vein (single

pulsating pattern during the heart cycle)

Figure 31.27: Highly pathological flow velocity waveforms of

the umbilical vein (double pulsating pattern during the heart

cycle)

Figure 31.28: Normal flow velocity waveforms of the

inferior vena cava (with reverse flow during the diastole)

end-CHAPTER 31 / Doppler Sonography in Obstetrics 511

nism of this increase is attributed to abnormal

ventri-cular filling characteristics, an abnormal ventriventri-cular wall

compliance, or abnormal end-diastolic pressure

Ductus Venosus (DV)

The DV transports oxygenated blood from the UV

directly through right atrium and foramen ovale to the

left atrium and ventricle, and then to the myocardium

and brain.100-106 The ductus venosus carries the most

rapidly moving blood in the venous system, and thus

is easily identifiable by the aliasing seen on Doppler

ultrasound The DV originates from the portal sinus

Thus, the frequently expressed concept that the DV

originates from the left portal vein or UV is anatomically

inaccurate.107 No anatomical continuity between the UV

and DV exists, as incorrectly described, in recent

Doppler ultrasound studies.108 It is well accepted that

the DV plays a major role in the regulation of fetal

circulation by modifying the volume of its flow

depending on the pressure gradient between the UV

and the heart.91

In normal fetuses, color Doppler demonstrates the

DV as a vessel bridging the left portal vein and the

inferior vena cava with an obvious gradient in velocity

compared with the left portal vein.91 A common error

is the sampling of the left hepatic vein rather than the

DV.75 Physiologically, this FVW shows continuous

forward flow during the heart cycle, mimicking the

pattern of the inferior vena cava (Figs 31.30 and 31.31)

The high pressure gradient between the UV and the

DV results in high blood flow velocities within this

vessel In contrast to other venous FVWs, reversed flow

in the DV is an abnormal finding, except for the firsttrimester due to the immaturity of the sphincter ofductus venosus However, abnormal FVWs of the DVbetween 11–14 weeks’ gestation was suggested to be ascreening test of fetal chromosomal abnormalities and/

or cardiac defects.109 Abnormal ductus venosus FVW(retrograde atrial-wave) is a strong predictor of fetalcardiac abnormality, may enhance the detection ofDown syndrome, is a good predictor of diverse causes

of fetal hydrops and may be a distant precursor ofsevere placenta-based IUGR.1

In IUGR fetuses, reversed flow in the DV is anominous sign (Figs 31.32 to 31.35) Reversed flow inthe ductus venosus results from a decline andsubsequent reversal in forward blood flow velocity

Figure 31.29: Abnormal flow velocity waveforms of the inferior

vena cava (with increasing reversed flow during end-diastole)

Figure 31.30: Visualization of the ductus venosus with color

Doppler and normal flow velocity waveforms (with forward flow during diastole and A-wave: corresponding to atrial contraction during the late diastole)

Figure 31.31: Normal flow velocity waveforms in the ductus

venosus (with forward flow during diastole and A-wave)

during atrial systole The abnormality in forwardcardiac function may be related to worsening placentaldisease, impaired cardiac function due to metaboliccompromise, redistribution of hepatoportal blood flowthrough the liver or a combination of these It wasreported that reverse flow patterns of the DV in IUGRfetuses is the only significant parameter associated withperinatal death.110

It has been suggested that changes in DV blood flowpattern precede the appearance of abnormal fetal heartrate patterns in pregnancies complicated with placentalinsufficiency.59,111 One should bear in mind, however,that these studies are technically difficult and that bloodflow patterns within the DV are also modulated by fetalbehavioral states, breathing movements and cardiacanomalies/arrhythmias.74,112,113

Timing of Delivery in Pregnancies Complicated with IUGR

The optimal timing of delivery in pregnancies cated by IUGR is still an issue to be resolved Clinicianshave to balance the risks of prematurity against the risks

compli-of prolonged fetal exposure to hypoxemia and acidemia,possibly resulting in fetal damage or death In a cross-sectional Doppler study of the fetal circulation, theappearance of significant changes in venous DopplerFVWs from the DV, inferior vena cava and hepatic veinswas observed after fetal arterial blood flow redistri-bution from the FDA to the MCA was established.59

Furthermore, the changes in the venous circulationseemed to be closely related to the onset of abnormalfetal heart rate patterns Reduced fetal heart ratevariation and occurrence of fetal heart rate decelerations

Figure 31.32: Initial pathological flow velocity waveforms of

the ductus venosus (with forward flow and decreasing

A-wave)

Figure 31.33: Abnormal flow velocity waveforms of the

ductus venosus (absent A-wave)

Figure 31.34: Highly pathological flow velocity waveforms

of the ductus venosus (reversed A-wave)

Figure 31.35: Highly pathological flow velocity waveforms

of the ductus venosus (pre-final situation)

CHAPTER 31 / Doppler Sonography in Obstetrics 513

have been associated with fetal hypoxemia,114 whereas

extremely low values of short-term variation were found

to be a reliable predictor of metabolic acidemia at

delivery or fetal death.115 In a longitudinal study,116 the

DV pulsatility index and short-term variation of

fetal-heart rate were found to be important indicators for

the optimal timing of delivery before 32 weeks’

gestation, and delivery was advised if one of these

parameters becomes persistently abnormal

In another study117 to determine time for delivery,

the changes in the hepatic vein, DV and UV were

investigated Results of this study suggested that adding

venous Doppler ultrasound to the arsenal of fetal

surveillance in IUGR fetuses might assist in timing of

delivery with less morbidity and mortality The venous

indices of the right hepatic vein and the DV, and double

UV pulsations were found to be the most useful tools

for this condition Finally it was stated that venous

Doppler evaluation could give valuable clinical

information for surveillance in high-risk pregnancies

In the recently published Growth Restriction

Inter-vention Trial study (GRIT: multicentered randomized

controlled trial) it was evaluated and compared if the

expectant management of the IUGR cases was superior

to the early delivery method.118 The main outcome was

death or disability at or beyond 2 years of age Overall

rate of death or severe disability at 2 years was 55 (19%)

of 290 immediate births and 44 (16%) of 283 delayed

births With adjustment for gestational age and

umbilical-artery Doppler category, the odds ratio (95%

CI) was 1.1 (0.7–1.8) Also the results of this study

guided clinicians minimally in constructing guidelines

for timing delivery in IUGR cases

UTEROPLACENTAL PERFUSION

In order to evaluate uteroplacental perfusion,

exami-nations performed at uterine arteries (UtA) give more

accurate information than the arcuate arteries.22

Velocities obtained from UtA are higher than from

arcuate arteries (Fig 31.36) This is important in

interpreting Doppler study results, and it should always

be paid attention on which vessel examinations were

performed

In the nonpregnant uterus, the UtA FVWs are

characterized by high impedance blood flow, and

almost always early diastolic notches Kurjak et al

reported the average UtA RI at the proliferative phase

to be 0.88 ± 0.04 (2SD).119 A high resistance to flow

during the midluteal phase of the cycle (day 21) has

been associated with infertility.120 In women undergoing

in vitro fertilization, those with a higher PI on the day

of follicular aspiration have a lower probability ofsuccessful pregnancy.121 Such findings suggest apotential value for UtA Doppler velocimetry inidentifying endometrial receptivity in infertile patients

In the first trimester, the intervillous maternalcirculation is established at 7 to 8 weeks.122 Theimpedance to blood flow within the intervillous spacesignificantly decreases towards the mid-pregnancy andthen remains stable Blood flow velocities are reaching

a plateau between 16 and 22 weeks of gestation, thenafter these parameters remain almost constant until the36th gestational week

From 6 to 12 weeks, FVWs obtained from the UtAare characterized by a high systolic and low diastoliccomponent (elevated S/D ratio), and the presence of anotch in the early diastolic period (Fig 31.37) Flowvelocity waveforms of the arcuate arteries also shownotching, but with a higher diastolic component.123 Inthe second and third trimester of pregnancy, the UtAdiameter enlarge,124 the systolic peak velocity andvolume flow rates increase,125,126 and a progressive fall

in impedance to blood flow can be detected.127 The earlydiastolic notch and the difference between S/D ratios

of the placental versus nonplacental sites shoulddisappear after 24–26 weeks’ gestation.125,128 Absence

of this transition from high to low impedance, and ofsimilar bilateral FVWs is associated with a higherincidence of hypertensive disease, abruption, intra-uterine fetal demise, preterm birth and IUGR

Blood flow velocities in uterine arteries depend onthe localization of placenta and gestational age.129 If theplacenta is laterally located, blood flow velocities in theipsilateral uterine artery are more important than the

Figure 31.36: Uterine and arcuate arteries,

visualized with color Doppler

flow velocities of the contralateral vessel Differences

between flow velocities of the right and left uterine

artery are evident at the early stages of pregnancy But

in the third trimester, the difference between the S/D

ratio of the vessels decrease to a minimum22 (Fig 31.38)

If an abnormal flow pattern is observed in the uterine

arteries, this most probably indicates the defective

perfusion of fetoplacental unit, which predicts a high

probability for developing preeclampsia, resulting with

intrauterine growth retardation5 (Fig 31.39)

At the early stages of pregnancy, end-diastolic flow

velocities in placental arteries are low, but systolic flow

is evident.22 With trophoblastic invasion and maturation

Figure 31.37: Normal flow velocity waveform of the

uterine artery in the first trimester (high resistance with an

early diastolic notch)

Figure 31.38: Normal flow velocity waveform in the

uterine artery in the third trimester (high end-diastolic flow,

without notching)

Figure 31.39: Abnormal flow velocity waveform in the

uterine artery in the third trimester (low end-diastolic flow, with an early diastolic notch)

Figure 31.40: Uterine arteries S/D ratio nomogram

Figure 31.41: Uterine arteries RI nomogram

CHAPTER 31 / Doppler Sonography in Obstetrics 515

Figure 31.42: Uterine arteries PI nomogram

of the uteroplacental vessels, beyond the second

trimester the high pressure system is converted to a low

pressure system, and vascular resistance declines.130 The

biologic variability after 20–24 weeks’ gestation becomes

almost stable (Figs 31.40 to 31.42)

Before 24 weeks’ gestation, early diastolic notching

due to the immature uteroplacental vascular system is

normally observed Beyond this gestational age,

persistent early diastolic notching is associated with

preeclampsia.7,10,12 Elevated RI, PI or S/D ratios and

the presence of a diastolic notch are considered as

abnormal UtA FVWs

Prediction of Complicated Pregnancies with

Uteroplacental Doppler Velocimetry

Pregnancies complicated with preeclampsia and IUGR

show evidence of impaired trophoblastic invasion and

maturation.131 A scoring system was proposed to predict

the chance of adverse outcomes (preeclampsia, IUGR,

preterm delivery, or fetal demise) using UtA Doppler

This score awarded 1 point for a notch and 1 point for

a low end-diastolic flow in each waveform, bilaterally

In example, a score of 4 would indicate bilaterally high

S/D ratios with bilateral notches Those with a score of

4 had an 83% rate of adverse perinatal outcomes, 48%

with a score of 3, 31% for a score of 2, and little increased

risk for a score of less than 2.132 Another group proposed

a two stage screening protocol for preeclampsia with

UtA Doppler at 18-22 weeks and when abnormal

re-evaluation at 24 weeks.5 In that study, 59% of the

re-examined patients showed normal UtA Doppler

FVWs.133 Persistence of an abnormal FVW increased the

relative risk for developing preeclampsia by 24-fold

Persistent notch in the early diastolic component of the

FVW increased the predictive value (from 4.3% to 28%)

and was associated with a 68-fold risk for developingpreeclampsia

There were also some studies suggesting Dopplerassessment of the UtA can be carried out at 11–14 weeks’gestation and that screening at this early gestation canalso identify pregnancies at the risk of developingcomplications associated with impaired placentation.134

Chromosomal defects are associated with IUGR,135 and

in the case of trisomy 18 and 13, but not in trisomy 21,the IUGR is evident from the first trimester of preg-nancy.136,137 In a study, in which UtA Doppler between11–14 weeks of gestation was performed to examinewhether the high lethality and IUGR is associated withchromosomal abnormalities, the authors showed thatUtA impedance is not associated with chromosomalanomalies,138 and suggested that the placentalhistological changes may be responsible for increasedimpedance in the UA, but not in the UtA

The relationship between abnormal uterine arteryDoppler velocimetry and preeclampsia, IUGR andadverse perinatal outcomes are well established Someparadoxical findings are attributed to differences inpatient selection, gestational ages for screening, type ofequipment, multiple definitions of FVWs, differentvessels examined and heterogeneous outcomecriteria.139 The sensitivity of the UtA examinationimproves as the gestational age approaches to 26 weeksand when persistent diastolic notch is one of the criteriafor analysis.140 However, whether its use as a routinescreening test ultimately results in a decrease inmaternal and perinatal morbidity and mortality remainsquestionable Current data do not support the use ofDoppler ultrasonography for routine screening ofpatients for preeclampsia However several studiesshow that the combination of the measurement ofuterine perfusion in the second trimester and analysis

of angiogenic markers have a high detection rate,especially for early onset preeclampsia.141 Among high-risk patients with a previous preeclampsia, UtA Dopplerhas an excellent negative predictive value, thus it is animportant tool in patient management and care which

is of paramount benefit for patients with preeclampsia

in a previous pregnancy A recently published tic review142 assessed the use of Doppler ultrasono-graphy in case of preeclampsia A total of 74 studies(69 cohort studies, 3 randomized controlled trials and

systema-2 case-control studies) with a total number of 79,547patients, of whom 2,498 developed preeclampsia, wereincluded The authors showed that UtA Doppler wasless accurate in the first trimester, than in the secondtrimester The combined data showed that the pulsatilityindex, alone or in combination with a persistent

notching after 24 weeks of gestation is the most

predictive parameter of Doppler ultrasonography to

predict preeclampsia

Although, considering the use of antiplatelet agent

prophylaxis during pregnancy, the results of some

multicenter randomized trials (Collaborative Low-Dose

Aspirin Study-CLASP143 and ECPPA144) were not

encouraging, a moderate but consistent reduction in the

relative risk of preeclampsia, of birth before 34 weeks’

gestation, and of having a pregnancy with a serious

adverse outcome.145 There is good evidence that

anti-platelet agents (principally low dose aspirin) prevent

moderate, but clinically important, reductions in the

relative risks of preeclampsia (19%), preterm birth (7%)

and perinatal mortality (16%) in women receiving

antiplatelet agents These effects are much smaller than

had initially been hoped for but, nevertheless,

poten-tially they have considerable public health importance

SUMMARY

Doppler ultrasound is a noninvasive technique that is

commonly used to evaluate maternal and fetal

hemodynamics Examination of fetomaternal vessels

using Doppler sonography has been subject of intensive

investigation in recent years To date, randomized

controlled trials were able to establish important clinical

value of Doppler velocimetry in obstetrics to improve

perinatal outcome in high risk situations Umbilical

artery, fetal descending aorta and middle cerebral artery

Doppler velocimetric studies are acceptable tools in the

diagnosis and management of intrauterine growth

restricted fetuses, and in the reduction of perinatal

mortality in high risk pregnancies But there is no

evidence that routine umbilical Doppler in a general or

low-risk population leads to any improvement in the

health of women or their infants Although other trials

are needed before asserting a definite lack of benefit,

umbilical Doppler examinations cannot be

recom-mended as a routine test in low-risk pregnancies

The majority of severely compromised fetuses also

show pathological venous velocimetry, which might

give valuable clinical information for surveillance in

high-risk pregnancies and their optimal perinatal

management In addition, Doppler sonography might

have a role in predicting long-term neuromotoric

outcome Large scale randomized controlled trials are

needed to establish the clinical utility of Doppler

ultrasound in obstetrics

REFERENCES

1 Harman CR, Baschat AA Comprehensive assessment of fetal wellbeing: which Doppler tests should be performed? Curr Opin Obstet Gynecol 2003;15(2):147-57.

2 Fitzgerald DE, Drumm JE Non-invasive measurement of human fetal circulation using ultrasound: a new method.

Br Med J 1977;2(6100):1450-1.

3 Campbell S, Diaz-Recasens J, Griffin DR, et al New Doppler technique for assessing uteroplacental blood flow Lancet 1983;1(8326 Pt 1):675-7.

4 Eik-Nes SH, Marsal K, Brubakk AO, et al Ultrasonic measurement of human fetal blood flow J Biomed Eng 1982;4(1):28-36.

5 Bower S, Schuchter K, Campbell S Doppler ultrasound screening as part of routine antenatal scanning: prediction

of pre-eclampsia and intrauterine growth retardation Br J Obstet Gynaecol 1993;100(11):989-94.

6 Caforio L, Testa AC, Mastromarino C, et al Predictive value

of uterine artery velocimetry at midgestation in low- and high-risk populations: a new perspective Fetal Diagn Ther 1999;14(4):201-5.

7 Campbell S, Pearce JM, Hackett G, et al Qualitative assessment of uteroplacental blood flow: early screening test for high-risk pregnancies Obstet Gynecol 1986;68(5): 649-53.

8 Harrington K, Cooper D, Lees C, et al Doppler ultrasound

of the uterine arteries: the importance of bilateral notching

in the prediction of pre-eclampsia, placental abruption or delivery of a small-for-gestational-age baby Ultrasound Obstet Gynecol 1996;7(3):182-8.

9 Harrington K, Goldfrad C, Carpenter RG, et al vaginal uterine and umbilical artery Doppler examination

Trans-of 12-16 weeks and the subsequent development Trans-of eclampsia and intrauterine growth retardation Ultrasound Obstet Gynecol 1997;9(2):94-100.

pre-10 Hoffmann H, Chaoui R, Bollmann R, et al [Potential clinical application of Doppler ultrasound in obstetrics] Zentralbl Gynakol 1989;111(19):1277-84.

11 Irion O, Massé J, Forest JC, et al Prediction of eclampsia, low birthweight for gestation and prematurity

pre-by uterine artery blood flow velocity waveforms analysis

in low risk nulliparous women Br J Obstet Gynaecol 1998;105(4):422-9.

12 Trudinger BJ, Giles WB, Cook CM Uteroplacental blood flow velocity-time waveforms in normal and complicated pregnancy Br J Obstet Gynaecol 1985;92(1):39-45.

13 Zimmermann P, Eiriö V, Koskinen J, et al D Doppler assessment of the uterine and uteroplacental circulation in the second trimester in pregnancies at high risk for pre- eclampsia and/or intrauterine growth retardation: comparison and correlation between different Doppler parameters Ultrasound Obstet Gynecol 1997;9(5):330-8.

14 Torloni MR, Vedmedovska N, Merialdi M, et al Safety of ultrasonography in pregnancy: WHO systematic review of the literature and meta-analysis Ultrasound Obstet Gynecol 2009;33(5):599-608.

CHAPTER 31 / Doppler Sonography in Obstetrics 517

15 Hershkovitz R, Sheiner E, Mazor M Ultrasound in

obstetrics: a review of safety Eur J Obstet Gynecol Reprod

Biol 2002;101(1):15-8.

16 Barnett SB, Kossoff G, Edwards MJ Is diagnostic

ultrasound safe? Current international consensus on the

thermal mechanism Med J Aust 1994;160(1):33-7.

17 Houston LE, Odibo AO, Macones GA The safety of

obstetrical ultrasound: a review Prenat Diagn 2009;29(13):

1204-12.

18 Newnham JP, Doherty DA, Kendall GE, et al Effects of

repeated prenatal ultrasound examinations on childhood

outcome up to 8 years of age: follow-up of a randomised

controlled trial Lancet 2004;364(9450):2038-44.

19 Mires GJ, Christie AD, Leslie J, et al Are ‘notched’ uterine

arterial waveforms of prognostic value for hypertensive

and growth disorders of pregnancy? Fetal Diagn Ther.

1995;10(2):111-8.

20 Deutinger J [Physiology of Doppler blood flow in maternal

blood vessels in pregnancy] Gynakologe

1992;25(5):284-91.

21 Fendel H, Fendel M, Pauen A, et al [Doppler studies of

arterial blood flow in the uterus during labor] Z

Geburtshilfe Perinatol 1984;188(2):64-7.

22 Fogarty P, Beattie B, Harper A, et al Continuous wave

Doppler flow velocity waveforms from the umbilical artery

in normal pregnancy J Perinat Med 1990;18(1):51-7.

23 Ertan AK, Hendrik HJ, Tanriverdi HA, et al Fetomaternal

Doppler sonography nomograms Clin Exp Obstet Gynecol.

2003;30(4):211-6.

24 Soothill PW, Ajayi RA, Campbell S, et al Prediction of

morbidity in small and normally grown fetuses by fetal

heart rate variability, biophysical profile score and

umbilical artery Doppler studies Br J Obstet Gynaecol.

1993;100(8):742-5.

25 Romero R, Kalache KD, Kadar N Timing the delivery of

the preterm severely growth-restricted fetus: venous

Doppler, cardiotocography or the biophysical profile?

Ultrasound Obstet Gynecol 2002;19(2):118-21.

26 Stuart B, Drumm J, Fitzgerald DE, et al Fetal blood velocity

waveforms in normal pregnancy Br J Obstet Gynaecol.

1980;87(9):780-5.

27 Thompson RS, Trudinger BJ, Cook CM Doppler ultrasound

waveform indices: A/B ratio, pulsatility index and

Pourcelot ratio Br J Obstet Gynaecol 1988;95(6):581-8.

28 Huneke B, Holst A, Schroder HJ, et al [Normal values for

relative Doppler indices A/B ratio, resistance index and

pulsatility index of the uterine artery and umbilical artery

in normal pregnancy A longitudinal study] Geburtshilfe

Frauenheilkd 1995;55(11):616-22.

29 Schulman H, Fleischer A, Stern W, et al Umbilical velocity

wave ratios in human pregnancy Am J Obstet Gynecol.

1984;148(7):985-90.

30 Trudinger BJ, Giles WB, Cook CM, et al Fetal umbilical

artery flow velocity waveforms and placental resistance:

clinical significance Br J Obstet Gynaecol

1985;92(1):23-30.

31 Maulik D, Yarlagadda AP, Youngblood JP, et al

Compo-nents of variability of umbilical arterial Doppler

velocimetry—a prospective analysis Am J Obstet Gynecol.

1989;160(6):1406-9.

32 Ertan AK, Hendrik HJ, Schmidt W Perinatologische Auffälligkeiten Bei Hochpathologischen Doppler-Flow- Befunden (Chapter 12) In: Schmidt W, Kurjak A (Eds) Farbdopplersonographie In Gynäkologie Und Geburtshilfe 1st edition Stuttgart: Thieme Verlag; 2000 pp 177-87.

33 Fleischer A, Schulman H, Farmakides G, et al Umbilical artery velocity waveforms and intrauterine growth retardation Am J Obstet Gynecol 1985;151(4):502-5.

34 Devoe LD, Gardner P, Dear C, et al The significance of increasing umbilical artery systolic-diastolic ratios in third- trimester pregnancy Obstet Gynecol 1992;80(4):684-7.

35 Rochelson B, Schulman H, Farmakides G, et al The significance of absent end-diastolic velocity in umbilical artery velocity waveforms Am J Obstet Gynecol 1987;156(5):1213-8.

36 Trudinger BJ, Cook CM, Giles WB, et al Fetal umbilical artery velocity waveforms and subsequent neonatal outcome Br J Obstet Gynaecol 1991;98(4):378-84.

37 Gudmundsson S, Marsal K Umbilical and uteroplacental blood flow velocity waveforms in pregnancies with fetal growth retardation Eur J Obstet Gynecol Reprod Biol 1988;27(3):187-96.

38 Baschat AA, Weiner CP Umbilical artery doppler screening for detection of the small fetus in need of antepartum surveillance Am J Obstet Gynecol 2000;182(1 Pt 1):154-8.

39 Mccowan LM, Harding JE, Stewart AW Umbilical artery doppler studies in small for gestational age babies reflect disease severity BJOG 2000;107(7):916-25.

40 Ertan AK, He JP, Tanriverdi HA, et al Comparison of perinatal outcome in fetuses with reverse or absent enddiastolic flow in the umbilical artery / fetal descending aorta J Perinat Med 2003;31(4):307-12.

41 Baschat AA, Gembruch U, Harman CR The Sequence of changes in Doppler and biophysical parameters as severe fetal growth restriction worsens Ultrasound Obstet Gynecol 2001;18(6):571-7.

42 Rizzo G, Pietropolli A, Capponi A, et al Chromosomal abnormalities in fetuses with absent end-diastolic velocity

in umbilical artery: analysis of risk factors for an abnormal karyotype Am J Obstet Gynecol 1994;171(3):827-31.

43 Ertan AK, He JP, Hendrik HJ, et al Perinatal events of cases with severely abnormal Doppler flow measurements J Perinat Med 2003; In Press.

44 Valcamonico A, Danti L, Frusca T, et al Absent diastolic velocity in umbilical artery: risk of neonatal morbidity and brain damage Am J Obstet Gynecol 1994;170(3):796-801.

end-45 Alfirevic Z, Neilson JP Doppler ultrasonography in risk pregnancies: systematic review with meta-analysis Am

high-J Obstet Gynecol 1995;172(5):1379-87.

46 Neilson JP, Alfirevic Z Doppler ultrasound for fetal assessment in high risk pregnancies Cochrane Database Syst Rev 2000;(2):CD000073.

47 Baschat AA, Gembruch U, Viscardi RM, et al Antenatal prediction of intraventricular hemorrhage in fetal growth restriction: what is the role of Doppler? Ultrasound Obstet Gynecol 2002;19(4):334-9.

48 Wienerroither H, Steiner H, Tomaselli J, et al Intrauterine blood flow and long-term intellectual, neurologic, and social development Obstet Gynecol 2001;97(3):449-53.

49 Ertan AK, Jost W, Hendrik HJ, et al Perinatal events and

neuromotoric development of children with zero flow in

the fetal vessels during the last trimester In: Cosmi E, Di

Renzo GC (Eds) 2nd World Congress of Perinatal

Medicine 1st edition Milano: Monduzzi Editore; 1993 pp.

1049-52.

50 Ertan AK, Jost W, Mink D, et al Neuromotoric

development of children after AED-flow during pregnancy.

In: Kurjak A, Latin V, Rippmann E (Eds) Advances On

The Pathophysiology Of Pregnancy 1st edition Milano:

CIC Edizioni Internazionali; 1995 pp 55-62.

51 Farrell T, Chien PF, Gordon A Intrapartum umbilical artery

doppler velocimetry as a predictor of adverse perinatal

outcome: a systematic review Br J Obstet Gynaecol.

1999;106(8):783-92.

52 Sijmons EA, Reuwer PJ, Van Beek E, et al The validity of

screening for small-for-gestational-age and

low-weight-for-length infants by Doppler ultrasound Br J Obstet Gynaecol.

1989;96(5):557-61.

53 Beattie RB, Dornan JC Antenatal screening for intrauterine

growth retardation with umbilical artery Doppler

ultrasonography BMJ 1989;298(6674):631-5.

54 Goffinet F, Paris-Llado J, Nisand I, et al Umbilical artery

Doppler velocimetry in unselected and low risk

pregnancies: a review of randomised controlled trials Br J

Obstet Gynaecol 1997;104(4):425-30.

55 Giles WB, Trudinger BJ, Cook CM, et al Umbilical artery

flow velocity waveforms and twin pregnancy outcome.

Obstet Gynecol 1988;72(6):894-7.

56 Gaziano EP, Knox H, Ferrera B, et al Is it time to reassess

the risk for the growth-retarded fetus with normal doppler

velocimetry of the umbilical artery? Am J Obstet Gynecol.

1994;170(6):1734-41.

57 Divon MY, Girz BA, Sklar A, et al Discordant twins—a

prospective study of the diagnostic value of real-time

ultrasonography combined with umbilical artery

velocimetry Am J Obstet Gynecol 1989;161(3):757-60.

58 Gaziano E, Gaziano C, Brandt D Doppler velocimetry

determined redistribution of fetal blood flow: correlation

with growth restriction in diamniotic monochorionic and

dizygotic twins Am J Obstet Gynecol

1998;178(6):1359-67.

59 Hecher K, Campbell S, Doyle P, et al Assessment of fetal

compromise by Doppler ultrasound investigation of the

fetal circulation Arterial, intracardiac, and venous blood

flow velocity studies Circulation 1995;91(1):129-38.

60 Senat MV, Schwarzler P, Alcais A, et al Longitudinal

changes in the ductus venosus, cerebral transverse sinus

and cardiotocogram in fetal growth restriction Ultrasound

Obstet Gynecol 2000;16(1):19-24.

61 Turan S, Miller J, Baschat AA Integrated testing and

management in fetal growth restriction Semin Perinatol.

2008;32(3):194-200.

62 Lingman G, Marsál K Fetal central blood circulation in

the third trimester of normal pregnancy—a longitudinal

study I Aortic and umbilical blood flow Early Hum Dev.

1986;13(2):137-50.

63 Hecher K, Spernol R, Szalay S, et al [Reference values for

the pulsatility index and the resistance index of blood flow

curves of the umbilical artery and fetal aorta in the 3d trimester] Ultraschall Med 1989;10(4):226-9.

64 Soothill PW, Nicolaides KH, Bilardo K, et al placental blood velocity resistance index and umbilical venous pO2, pCO2, pH, lactate and erythroblast count in growth-retarded fetuses Fetal Ther 1986;1(4):176-9.

Utero-65 Jouppila P, Kirkinen P Blood velocity waveforms of the fetal aorta in normal and hypertensive pregnancies Obstet Gynecol 1986;67(6):856-60.

66 Laurin J, Lingman G, Marsal K, et al Fetal blood flow in pregnancies complicated by intrauterine growth retardation Obstet Gynecol 1987;69(6):895-902.

67 Hackett GA, Campbell S, Gamsu H, et al Doppler studies

in the growth retarded fetus and prediction of neonatal necrotising enterocolitis, haemorrhage, and neonatal morbidity Br Med J (Clin Res Ed) 1987;294(6563):13-6.

68 Arabin B, Siebert M, Jimenez E, et al Obstetrical characteristics of a loss of end-diastolic velocities in the fetal aorta and/or umbilical artery using Doppler ultrasound Gynecol Obstet Invest 1988;25(3):173-80.

69 Tonge HM, Wladimiroff JW, Noordam MJ, et al Blood flow velocity waveforms in the descending fetal aorta: comparison between normal and growth-retarded pregnancies Obstet Gynecol 1986;67(6):851-5.

70 Bonatz G, Schulz V, Weisner D, et al Fetal Heart rate (fhr) pathology in labor related to preceeding Doppler sonographic results of the umbilical artery and fetal aorta

in appropriate and small for gestational age babies A Longitudinal Analysis J Perinat Med 1997;25(5):440-6.

71 Marsal K, Laurin J, Lindblad A, et al Blood flow in the fetal descending aorta Semin Perinatol 1987;11(4):322-34.

72 Ley D, Laurin J, Bjerre M, et al Abnormal fetal aortic velocity waveform and minor neurological dysfunction at

7 years of age Ultrasound Obstet Gynecol 9.

1996;8(3):152-73 Ley D, Tideman E, Laurin J Abnormal fetal aortic velocity waveform and intellectual function at 7 years of age Ultrasound Obstet Gynecol 1996;8(3):160-5.

74 Divon MY, Ferber A Doppler Evaluation of the fetus Clin Obstet Gynecol 2002;45(4):1015-25.

75 Mari G, Detti L Doppler ultrasound application to fetal medicine (Chapter 12) In: Fleischer A, Manning F, Jeanty

P, Romero R (Eds) Sonography in obstetrics and gynecology (Principles and Practice) 6th edition New York, USA: Mcgraw Hill; 2001 pp 247-83.

76 Mari G, Moise KJ, Deter RL, et al Doppler assessment of the pulsatility index in the cerebral circulation of the human fetus Am J Obstet Gynecol 1989;160(3):698-703.

77 Vetter K [The significance of Doppler blood flow measurement in recognizing placental insufficiency] Arch Gynecol Obstet 1988;244 Suppl:S12-S18.

78 Arabin B, Bergmann PL, Saling E Simultaneous assessment

of blood flow velocity waveforms in uteroplacental vessels, the umbilical artery, the fetal aorta and the fetal common carotid artery Fetal Ther 1987;2:17-26.

79 Strigini FA, De Luca G, Lencioni G, et al Middle cerebral artery velocimetry: different clinical relevance depending

on umbilical velocimetry Obstet Gynecol 7.

1997;90(6):953-CHAPTER 31 / Doppler Sonography in Obstetrics 519

80 Sepulveda W, Shennan AH, Peek MJ Reverse

end-diastolic flow in the middle cerebral artery: an agonal

pattern in the human fetus Am J Obstet Gynecol.

1996;174(5):1645-7.

81 Vyas S, Nicolaides KH, Bower S, et al Middle cerebral

artery flow velocity waveforms in fetal hypoxaemia Br J

Obstet Gynaecol 1990;97(9):797-803.

82 Mari G, Adrignolo A, Abuhamad AZ, et al Diagnosis of

fetal anemia with Doppler ultrasound in the pregnancy

complicated by maternal blood group immunization.

Ultrasound Obstet Gynecol 1995;5(6):400-5.

83 Mari G, Deter RL, Carpenter RL, et al Noninvasive

diagnosis by Doppler ultrasonography of fetal anemia due

to maternal red-cell alloimmunization Collaborative Group

for Doppler Assessment of the Blood Velocity in Anemic

Fetuses N Engl J Med 2000;342(1):9-14.

84 Zimmerman R, Carpenter RJ, Durig P, et al Longitudinal

measurement of peak systolic velocity in the fetal middle

cerebral artery for monitoring pregnancies complicated by

red cell alloimmunisation: a prospective multicentre trial

with intention-to-treat BJOG 2002;109(7):746-52.

85 Moise KJ The usefulness of middle cerebral artery Doppler

assessment in the treatment of the fetus at risk for anemia.

Am J Obstet Gynecol 2008;198(2):161-4.

86 Mari G, Detti L, Oz U, et al Accurate prediction of fetal

hemoglobin by Doppler ultrasonography Obstet Gynecol.

2002;99(4):589-93.

87 Huisman TW Doppler assessment of the fetal venous

system Semin Perinatol 2001;5(1):21-31.

88 Laurichesse-Delmas H, Grimaud O, Moscoso G, et al Color

Doppler study of the venous circulation in the fetal brain

and hemodynamic study of the cerebral transverse sinus.

Ultrasound Obstet Gynecol 1999;13(1):34-42.

89 Yoshimura S, Masuzaki H, Miura K, et al Diagnosis of

fetal pulmonary hypoplasia by measurement of blood flow

velocity waveforms of pulmonary arteries with Doppler

ultrasonography Am J Obstet Gynecol 1999;180(2 Pt

1):441-6.

90 Hoffman C, Galan HL Assessing the ‘at-risk’ fetus: Doppler

ultrasound Curr Opin Obstet Gynecol 2009;21(2):161-6.

91 Contratti G, Banzi C, Ghi T, et al Absence of the ductus

venosus: report of 10 new cases and review of the literature.

Ultrasound Obstet Gynecol 2001;18(6):605-9.

92 Arduini D, Rizzo G, Romanini C The development of

abnormal heart rate patterns after absent end-diastolic

velocity in umbilical artery: analysis of risk factors Am J

Obstet Gynecol 1993;168(1 Pt 1):43-50.

93 Damron DP, Chaffin DG, Anderson CF, et al Changes in

umbilical arterial and venous blood flow velocity

waveforms during late decelerations of the fetal heart rate.

Obstet Gynecol 1994;84(6):1038-40.

94 Reed K, Chaffin DG, Anderson CF, et al Umbilical venous

pulsations are related to atrial contraction pressure

waveforms in fetal lambs Obstet Gynecol 1997;89:953-6.

95 Ferrazzi E, Rigano S, Bozzo M, et al Umbilical vein blood

flow in growth-restricted fetuses Ultrasound Obstet

Gynecol 2000;16(5):432-8.

96 Gudmundsson S, Huhta JC, Wood DC, et al Venous

Doppler ultrasonography in the fetus with nonimmune

hydrops Am J Obstet Gynecol 1991;164(1 Pt 1):33-7.

97 Nakai Y, Miyazaki Y, Matsuoka Y Pulsatile umbilical venous flow and its clinical significance Br J Obstet Gynaecol 1992;99(12):977-80.

98 Chan FY, Woo SK, Ghosh A, et al Prenatal diagnosis of congenital fetal arrhythmias by simultaneous pulsed Doppler velocimetry of the fetal abdominal aorta and inferior vena cava Obstet Gynecol 1990;76(2):200-5.

99 Rizzo G, Arduini D, Romanini C Inferior vena cava flow velocity waveforms in appropriate and small-for gesta- tional age fetsues Am J Obstet Gynecol 1992;166:1271-80.

100 Kiserud T, Eik-Nes SH, Blaas HG, et al Ultrasonographic velocimetry of the fetal ductus venosus Lancet 1991;338(8780):1412-4.

101 Kiserud T, Hellevik LR, Eik-Nes SH, et al Estimation of the pressure gradient across the fetal ductus venosus based

on Doppler velocimetry Ultrasound Med Biol 1994;20(3):225-32.

102 Kiserud T In a different vein: the ductus venosus could yield much valuable information Ultrasound Obstet Gynecol 1997;9(6):369-72.

103 Kiserud T, Rasmussen S How repeat measurements affect the mean diameter of the umbilical vein and the ductus venosus Ultrasound Obstet Gynecol 1998;11(6):419-25.

104 Kiserud T, Crowe C, Hanson M Ductus venosus agenesis prevents transmission of central venous pulsations to the umbilical vein in fetal sheep Ultrasound Obstet Gynecol 1998;11(3):190-4.

105 Kiserud T Ductus venosus blood velocity in myeloproliferative disorders Ultrasound Obstet Gynecol 2001;18(2):184-5.

106 Kiserud T The ductus venosus Semin Perinatol 2001;25(1):11-20.

107 Mavrides E, Moscoso G, Carvalho JS, et al The anatomy

of the umbilical, portal and hepatic venous systems in the human fetus at 14-19 weeks of gestation Ultrasound Obstet Gynecol 2001;18(6):598-604.

108 Bellotti M, Pennati G, De Gasperi C, et al Role of ductus venosus in distribution of umbilical blood flow in human fetuses during second half of pregnancy Am J Physiol Heart Circ Physiol 2000;279(3):H1256-63.

109 Matias A, Montenegro N Ductus venosus blood flow in chromosomally abnormal fetuses at 11 to 14 weeks of gestation Semin Perinatol 2001;25(1):32-7.

110 Ozcan T, Sbracia M, d’Ancona RL, et al Arterial and venous doppler velocimetry in the severely growth-restricted fetus and associations with adverse perinatal outcome Ultrasound Obstet Gynecol 1998;12(1):39-44.

111 Hecher K, Hackeloer BJ Cardiotocogram compared to Doppler investigation of the fetal circulation in the premature growth-retarded fetus: longitudinal observations Ultrasound Obstet Gynecol 1997;9(3):152-61.

112 Kiserud T Fetal venous circulation—an update on hemodynamics J Perinat Med 2000;28:90-6.

113 Kiserud T Liver length in the small-for-gestational-age fetus and ductus venosus flow Am J Obstet Gynecol 2000;182(1 Pt 1):252-3.

114 Ribbert L, Snijders RJ, Nicolaides KH Relation of fetal blood gases and data from computer assisted analysis of fetal heart rate patterns Br J Obstet Gynaecol 1991;98(8): 820-3.

115 Dawes GS, Moulden M, Redman C Short-term fetal heart

rate variation, decelerations, and umbilical flow velocity

waveforms before labor Obstet Gynecol 1992;80(4):673-8.

116 Hecher K, Bilardo CM, Stigter RH, et al Monitoring of

fetuses with intrauterine growth restriction: a longitudinal

study Ultrasound Obstet Gynecol 2001;18(6):564-70.

117 Hofstaetter C, Gudmundsson S, Hansmann M Venous

Doppler velocimetry in the surveillance of severely

compromised fetuses Ultrasound Obstet Gynecol 2002;

20(3):233-9.

118 Thornton JG, Hornbuckle J, Vail A, et al; the GRIT study

group Infant wellbeing at 2 years of age in the Growth

Restriction Intervention Trial (GRIT): multicentred

randomised controlled trial Lancet 2004;364(9433):513-20.

119 Kurjak A, Kupesic-Urek S, Schulman H, et al Transvaginal

color flow Doppler in the assessment of ovarian and uterine

blood flow in infertile women Fertil Steril 1991;56(5):870-3.

120 Deutinger J, Rudelstorfer R, Bernaschek G

Vaginosono-graphic Doppler velocimetry in both uterine arteries:

elevated left-right differences and relationship to fetal

haemodynamics and outcome Early Hum Dev 1991;25(3):

187-96.

121 Goswamy R, Williams G, Steptoe P Decreased uterine

per-fusion—a cause of infertility Hum Reprod 1989;3(8):955-9.

122 Kurjak A, Dudenhausen JW, Hafner T, et al Intervillous

circulation in all three trimesters of normal pregnancy

assessed by color Doppler J Perinat Med 1997;25(4):373-80.

123 Coppens M, Loquet P, Kollen M, et al Longitudinal

evaluation of uteroplacental and umbilical blood flow

changes in normal early pregnancy Ultrasound Obstet

Gynecol 1996;7(2):114-21.

124 Thaler I, Manor D, Itskovitz J, et al Changes in uterine

blood flow during human pregnancy Am J Obstet Gynecol.

1990;162(1):121-5.

125 Kofinas AD, Espeland MA, Penry M, et al Uteroplacental

Doppler flow velocity waveform indices in normal

preg-nancy: a statistical exercise and the development of

appro-priate reference values Am J Perinatol 1992;9(2):94-101.

126 Palmer SK, Zamudio S, Coffin C, et al Quantitative

estimation of human uterine artery blood flow and pelvic

blood flow redistribution in pregnancy Obstet Gynecol.

1992;80(6):1000-6.

127 den Ouden M, Cohen-Overbeek TE, Wladimiroff JW.

Uterine and fetal umbilical artery flow velocity waveforms

in normal first trimester pregnancies Br J Obstet Gynaecol.

1990;97(8):716-9.

128 Tekay A, Jouppila P A longitudinal Doppler

ultrasonographic assessment of the alterations in peripheral

vascular resistance of uterine arteries and ultrasonographic

findings of the involuting uterus during the puerperium.

Am J Obstet Gynecol 1993;168(1 Pt 1):190-8.

129 Schneider KT, Loos W [The 10th anniversary of obstetric

Doppler sonography—development and perspectives].

Geburtshilfe Frauenheilkd 1989;49(5):407-15.

130 Brosens I, Dixon HG, Robertson W Fetal growth

retardation and the arteries of the placental bed Br J Obstet

Gynaecol 1977;84(9):656-63.

131 Hitschold T, Ulrich S, Kalder M, ET AL [Blood flow profile

in the uterine artery Correlation with placental

morpho-logy and clinico-obstetrical data within the scope of eclampsia] Z Geburtshilfe Neonatol 1995;199(1):8-12.

pre-132 Murakoshi T, Sekizuka N, Takakuwa K, et al Uterine and spiral artery flow velocity waveforms in pregnancy- induced hypertension and/or intrauterine growth retardation Ultrasound Obstet Gynecol 1996;7(2):122-8.

133 Bower S, Bewley S, Campbell S Improved prediction of preeclampsia by two-stage screening of uterine arteries using the early diastolic notch and color Doppler imaging Obstet Gynecol 1993;82(1):78-83.

134 Martin AM, Bindra R, Curcio P, Cicero S, Nicolaides KH Screening for pre-eclampsia and fetal growth restriction

by uterine artery Doppler at 11-14 weeks of gestation Ultrasound Obstet Gynecol 2001;18(6):583-6.

135 Snijders RJ, Sebire NJ, Cuckle H, et al Maternal age and gestational age-specific risks for chromosomal defects Fetal Diagn Ther 1995;10(6):356-67.

136 Kuhn P, Brizot ML, Pandya PP, et al Crown-rump length

in chromosomally abnormal fetuses at 10 to 13 weeks’ gestation Am J Obstet Gynecol 1995;172(1 Pt 1):32-5.

137 Schemmer G, Wapner RJ, Johnson A, et al First trimester growth patterns of aneuploid fetuses Prenat Diagn 1997;17(2):155-9.

138 Bindra R, Curcio P, Cicero S, et al Uterine artery Doppler

at 11-14 weeks of gestation in chromosomally abnormal fetuses Ultrasound Obstet Gynecol 2001;18(6):587-9.

139 Goncalves LF, Romero R, Gervasi M, et al Doppler velocimetry of the uteroplacental circulation (Chapter 13) In: Fleischer A, Manning F, Jeanty P, Romero R (Eds) Sonography in Obstetrics and Gynecology (Principles And Practice) 6th edition New York, USA: Mcgraw Hill; 2001.

pp 285-313.

140 Newnham JP, Patterson LL, James IR, et al An evaluation

of the efficacy of Doppler flow velocity waveform analysis

as a screening test in pregnancy Am J Obstet Gynecol 1990;162(2):403-10.

141 Grill S, Rusterholz C, Zanetti-Dällenbach R, et al Potential markers of preeclampsia—a review Reprod Biol Endocrinol 2009;7:70.

142 Cnossen JS, Morris RK, ter Riet G, et al Use of uterine artery Doppler ultrasonography to predict pre-eclampsia and intrauterine growth restriction: a systematic review and bivariable meta-analysis CMAJ 2008;178(6):701-11.

143 CLASP: a randomised trial of low-dose aspirin for the prevention and treatment of pre-eclampsia among 9364 pregnant women CLASP (Collaborative Low-dose Aspirin Study in Pregnancy) Collaborative Group Lancet 1994;343(8898):619-29.

144 ECPPA: randomised trial of low dose aspirin for the prevention of maternal and fetal complications in high risk pregnant women ECPPA (Estudo Colaborativo para Prevenção da Pré-eclampsia com Aspirina) Collaborative Group Br J Obstet Gynaecol 1996;103(1):39-47.

145 Askie LM, Duley L, Henderson-Smart DJ, et al Antiplatelet agents for prevention of pre-eclampsia: a meta-analysis of individual patient data Lancet 2007;369(9575):1791-8.

146 Duley L, Henderson-Smart DJ, Knight M, et al Antiplatelet agents for preventing pre-eclampsia and its complications Cochrane Database Syst Rev 2004;(1):CD004659.

as a main characteristic of the puerperium was previously assessed by palpation of the fundal height.

Since the introduction of ultrasound (USG) in clinical practice by Ian Donald et al.2 in 1958 the uterusbecame one of the first organs to be examined.3-7 However, few studies have focused on USG investigationsduring the puerperium and results of published studies are not unambiguous.1-16 In published studies concerningthe involution process, the length,4,6-9,11,12,14 width,8,9,12 anteroposterior diameter,3-7,11-13,16 area,9 thickness ofthe uterine wall10 and volume of the uterus and the uterine cavity,15 have been used as a measure of uterineinvolution Majority of the studies described pathological conditions without knowledge about normal findings,4,5,8

they were restricted to the early puerperium and designs were cross-sectional.3-7,12 A few studies concerninguterine cavity during normal puerperium have been published.13-16

Postpartum complications involving the uterus occur in about 8–10% of cases Immediate and late postpartumhemorrhage, puerperal sepsis, and septic pelvic thromboembolism are still potentially life-threatening conditions.Abnormal placentation (placenta accreta, increta or percreta) is a rare cause of postpartum hemorrhage thatmay continue after delivery Several studies investigated antenatal ultrasound diagnosis of this condition17-23

but a few papers have focused on postpartum ultrasound monitoring of retained placenta accreta.24 Ultrasoundcan help to diagnose vascular lesions, congenital or acquired,25-31 placental site tumor32 and choriocarcinoma,which can also cause severe postpartum hemorrhage

Thus, whenever puerperal complication occurs, the obstetricians should not hesitate to switch on ultrasoundmachine

NORMAL PUERPERIUM

A description of normal ultrasound changes of the

uterus and uterine cavity during puerperium is a

prerequisite for ultrasound diagnosis of pathological

conditions We can follow the physiological involution

of the uterus weighing more than 1 kg soon after

delivery to an organ weighing about 80 grams at the

end of the puerperium by means of ultrasound Theinvolution changes concerning the size, shape, positionand texture of the uterus have been relatively wellexamined by ultrasound.3-16 The influence on theinvolution process of parity,7,9,11,13,15,16 route ofdelivery,11 oxytocin administration during labor7 breast-feeding6,7,9, 11-13,15,16 or the infant’s weight11-13 havebeenstudied Previously published studies involving

sonographic examination of uterine cavity are not

unambiguous.6,11,13-16

In the early and middle puerperium (in the first

2 weeks) the transabdominal approach is to be

recommended A relatively short focal length of the

vaginal probe limits its use during the early postpartum

period, when the uterus is too large and lies near the

abdominal wall In contrast, during the late postpartum

period (> 2weeks) a high frequency transvaginal probe,

which better distinguishes minor details, should be

used At that time, the uterus is considerably decreased

in size and it lies in the true pelvis The postpartum

uterus should be examined in three standard sections:

sagittal, transverse and coronal (Figs 32.1 and 32.2)

Urinary bladder should be moderately filled Gentle

compression with the probe should be used in order to

avoid uterine distortion

We can differentiate three typical ultrasound images

during normal puerperium: in the early, middle and

late puerperium (Figs 32.3 and 32.4) The involution of

the uterus is a dynamic process that has no parallel

process in normal adult life.1 There are two

physio-logical life-saving processes occurring soon after

The appearance of ultrasound finding in the early

postpartum period reflects these physiological changes

The uterus has an angulated form (Fig 32.4A) It lies in

a slightly retroflexed position and arches over the sacral

promontory Wachsberg et al.12 pointed out the impact

of uterine angulation on the measurement of uterine

length and recommended segmental measurement This

angulated form of the early puerperal uterus is typical

only in early puerperium and it is artificial An

extremely great degree of uterine deformability is

caused by a heavy uterine corpus, a hypotonic lower

Figures 32.1A to C: Three standard ultrasound sections of

the puerperal uterus (A) Longitudinal; (B) Coronal;

(C) Transverse

Figures 32.2A to C: Transabdominal ultrasound scans of a

normal puerperal uterus on day 1 (A) Longitudinal scan; (B) Coronal scan; (C) Transverse scan

Figures 32.3A to C: The normal ultrasound appearance of

the uterus and uterine cavity during the puerperium (A) Transabdominal approach during the early puerperium; (B) During the middle part of the puerperium; (C) Transvaginal approach during the late puerperium

CHAPTER 32 / Postpartum Ultrasound 523

uterine segment and supine position of the examined

woman Lifesaving uterine contraction approaches

anterior and posterior uterine walls and just a virtual

cavity appears The uterine cavity is empty and decidua

appears as a thin white line from the fundus to the level

of the internal cervical os (Fig 32.4A) Sometimes, this

line can be irregular and thicker, which probably

depends on the amount of retained decidua (Fig 32.5A)

The separation of the placenta and membranes generallyoccurs in the spongy layer; however the level varies In

1931, Williams wrote concerning the line of separation

of the placenta and membranes: “While separationgenerally occurs in the spongy layer, the line is very irregular

so that in places a thick layer of decidua is retained, in othersonly a few layers of cells remain, while in still others themuscularis is practically bare.”33 The variation in

Figures 32.4A to C: Three typical USG images during normal puerperium (A) In the early puerperium: uterus is retroverted.

The cavity is seen as a thin white line; (B) In the middle puerperium: uterus is anteverted An abundant fluid or mixed echo pattern with echogenic and echo-free area is seen in the whole cavity; (C) In the late puerperium: uterus is considerably decreased in size; the cavity is empty and appears as a thin white line

Figures 32.5A to D: Transabdominal, longitudinal scans of the uterus from an uncomplicated

puerperium (A) On day 1; (B) On day 7; (C) On day 14; (D) On day 28

sonographic appearance of the cavity could be seen as

a demonstration of these physiological variations in

retained decidua The white thin line seen on ultrasound

might possibly represent cases in which only the basal

decidual layer is retained or if the muscularis is

practically bare (Fig 32.4A) Whereas the thicker and

more irregular lines might represent cases with retention

of more amount of spongy decidual layer and perhaps

fragments of membranes (Fig 32.5A)

Fluid or echogenic mass is not common finding in

the cavity in the early postpartum period.13 Small

echogenic or echolucent dots in the cavity are harmless

physiological findings.13,34 A heterogeneous mass with

fluid and solid components can be seen in the cervical

area.13,14,34,35 This finding has no clinical significance and

the mass is usually expelled spontaneously It probably

reflects a collection of blood, blood clots and parts of

membranes On the posterior wall of the uterus the

prominent uterine vascular channels are regularly

seen.11 They usually disappear during the 2nd and 3rd

postpartum weeks as a result of involution process,

which decreases both the size and the amount of uterine

vessels Gas in the cavity is not common finding in the

early postpartum period although it can be occasionally

seen.13 Wachsberg detected gas in 19% of normal

population during the early postpartum period.36

In the middle part of the puerperium (1–2 weeks

postpartum) the uterus is diminished, the shape of the

uterus is oval It rotates along its internal cervical os

towards an anteflexed position probably due to forming

a firm isthmus.13 The vascular channels are not so

prominent Either pure fluid or mixed echo with fluid

and solid components can be seen in the whole cavity

not only in the cervical area (Figs 32.4B and 32.5B and

C) This finding reflects a normal healing process of the

placental site inside uterine cavity, necrotic changes ofretained decidua and an abundant shedding of lochia.Echogenic mass or gas is not common finding duringmiddle part of the puerperium In contrast Edwards,

et al.15 found an echogenic mass in a great proportion

of normal puerperal women

During late puerperium (>2 weeks postpartum), the uterus

is considerably diminished (Figs 32.4C and 32.5D) Itlies in an anteflexed position in 88% of cases.13 In 12 %

of cases the uterus has a retroflexed position ponding well to normal prevalence of retroversion ofthe uterus in general population (Fig 32.6A) Theuterine cavity is again empty Decidua and necroticvessel ends are exfoliated, the placental site is recoveredand a new endometrium is regenerated from the basallayer of the decidua adjacent to the myometrium.Ultrasonically the cavity in the late puerperium appears

as a thin white line (Figs 32.4C and 32.5D) This ponds to an inactive endometrium and reflects thehypoestrogenic state of the puerperium (“the physio-logic menopause”) Sometimes, a small amount of fluid

corres-or echogenic dots can be seen (arrow) (Fig 32.6B)

In 1953, Sharman performed endometrium biopsiesand identified fully restored endometrium from the 16thpostpartum day.37 In contrast, a study published in 1986

by Oppenheimer38 showed that duration of puerperallochia may be up to 60 days in 13% of women Similarly

in a recently published study,39 on the duration ofpostpartum bleeding among 477 breastfeeding women,

it was reported that the median duration of lochia was

27 days with a range from 5 to 90 days Only 15% ofthe women reported that their lochia had stoppedwithin two weeks postpartum They also pointed to thefact that bleeding associated with the postpartumhealing process commonly stops and starts again So,

Figures 32.6A and B.: (A) Transvaginal ultrasound image of the uterus on day 28 postpartum shows a retroverted uterus on

day 28 postpartum; (B) Transvaginal ultrasound image of the uterus on day 28 postpartum shows a small amount of fluid

with echogenic foci in the cavity (white arrow)

CHAPTER 32 / Postpartum Ultrasound 525

the normal physiological time span for the placental site

to recover is probably 4–6 weeks and not two weeks as

previously considered

Doppler Ultrasound During Normal Puerperium

Besides conventional ultrasound, Doppler technology

is used to study hemodynamic events occurring during

the puerperium Normal pregnancy requires the growth

of many new vessels Consequently, during puerperium

dramatically regressive changes must occur The

physiological involution of the uterus involves not only

muscle cells and decidua but also the arteries From

histological studies, we know that normal involuted

placental bed is characterized by a disappearance of

trophoblasts and completely thrombosed spiral

arteries.40-42 High diastolic flow velocities in

combi-nation with a disappearance of the early diastolic notch

are the main characteristics of the uterine artery Doppler

flow pattern from gestational week 20–26 and they

reflect the physiological conversion from high

(non-pregnant) to low ((non-pregnant) resistance state.43,44 How

fast these physiological changes return to the

non-pregnant state is a controversial issue.45-48 Tekay and

Jouppila14 assessed the peripheral vascular resistance

of the uterine arteries in 42 postpartum women and

found that the pulsatility index (PI) increased

signi-ficantly in early puerperium compared to pregnancy,

remained unchanged during the next six weeks and

then gradually started to increase again However,

non-pregnant values were not reached even three months

after delivery Jaffa et al.,46 on the other hand, described

that PI decreased in the 2nd and remained relatively

low until the 4th postpartum week Similar differences

regarding the reappearance of the early diastolic notch

have been reported Tekay and Jouppila14 noted areappearance of the early diastolic notch already in earlypuerperium in 40 of 42 women, while Jaffa et al.46 foundthat the early diastolic notch had reappeared in onlyone of 60 women five weeks postpartum

According to our findings,48 in early puerperium themeans of Doppler flow resistance indices are higherthan those reported in late pregnancy Thereafter, they

do not change markedly until day 28 postpartum Onday 56 postpartum, they are still lower compared tothe values reported for nonpregnant women, whichspeaks for longer duration of physiological vascularreturn from a pregnant to a nonpregnant state Weobserved a diastolic notch in 13% of women on dayone and in 90.6% of women on day 56 postpartum(Figs 32.7A and B)

Color and power Doppler ultrasound may detect alocalized area of increased vascularity within themyometrium It may be a common transient ultrasoundfinding if asymptomatic and it does not requiretreatment.47

THREE-DIMENSIONAL ULTRASOUND POSTPARTUM

Although the volume of the uterus and uterine cavitywere previously measured using 2D ultrasound,15 thevolumes assessed by 3D (three-dimensional) ultrasoundmay provide more accurate measurements than doesthe conventional ultrasound 3D ultrasound usingVOCAL program (Virtual Organ Computer-aidedAnalysis) has recently been used to measure thevolumes of the uterus and the uterine cavity afternormal delivery.49 It is shown in Figures 32.8A and B

Figures 32.7A and B: (A) Normal flow velocity waveforms of the uterine artery on day 1

(Transabdominal approach) and; (B) 56 (Transvaginal approach) postpartum

3D power Doppler angiography is a new unexplored

method for quantifying noninvasively the vascular

network of the uterus (Fig 32.8C)

RETAINED PLACENTAL TISSUE

Both ultrasound diagnosis of RPT (retained placental

tissue) and appropriate management for SPH

(secon-dary postpartum hemorrhage) is still a controversial

issue SPH is defined as any abnormal bleeding from

the uterus occurring between 24 hours and 12 weeks

postpartum49 and occurs in 1–2% of deliveries.50,51 In

developed countries, half of postpartum women who

are admitted to hospital with this condition undergo

uterine surgical evacuation.49-53 In developing countries,

it is a major contributor to maternal death.49 The most

common causes of SPH are abnormal involution of the

placental site in the uterine cavity that may be

idio-pathic42 or it can be caused by RPT54 or by

endo-metritis.52 Subinvolution of the placental bed in the

absence of RPT or endometritis is a distinctive entity,

characterized by widely distended spiral arteries, only

partly occluded by thrombi of various ages and invested

with extravillous trophoblasts.40,42 The diagnosis,

however, requires histological examination and

clinically it is a diagnosis of exclusion Moreover,

placental vascular subinvolution is often

under-recognized by general surgical pathologists.42 Carlan et

al.55 performed manual exploration of the cavity on 131

asymptomatic women, five minutes after placental

delivery and within two minutes after an ultrasound

examination They found that 24 of 131(18.8%) women

had documented evidence of RPT This is a surprisingly

higher figure compared to Jones et al.56 who performed

manual intrauterine explorations routinely after 1000

births and removed placental fragments or bits of

membranes in only 2–4% of cases Defective decidua,

which can be scanty or completely absent in some

patients, is a predisposing factor for abnormalattachment of the placenta and for partially RPT.40

Vascular abnormalities of the uterus have recently beendescribed as possibly more common causes of severeSPH than previously thought.25-31

In a Cochrane Review, Alexander et al.50 identified

45 papers about the management of SPH and concludedthat little information is available from randomizedtrials to guide clinicians in the management of thiscondition Since the causes of SPH may be numerous,the best treatment options should be chosen according

to the underlying cause of bleeding However, anessential problem is that the underlying cause of SPHoften is unknown and that clinical or ultrasounddiagnosis of RPT, which is the indication for surgicaltreatment, is still a controversial issue.58-68 The decisionwhether to perform uterine evacuation for RPT depends

on both, clinical finding and the ability to visualizeretained placenta by ultrasound.58-69 Although promptcurettage seems to be necessary, in many cases it usuallydoes not remove identifiable placental tissue Moreover,

it is more likely to traumatize the implantation site andincite more bleeding Consequently, the complicationsrate is high Hoveyda et al reported in his reviewregarding secondary postpartum hemorrhage that thefrequency of perforation of the uterus was 3% andhysterectomy about 1%.54 Similar results are reportedfrom an audit of 200 cases concerning puerperalcurettage.70 They showed that 8.5% of patientsexperienced major morbidity and 7% required a repeatprocedure with further morbidity In addition toimmediate complications, late sequelae related tosurgical treatment for SPH may influence the repro-ductive health of women If curettage damages theendometrium 1–4 weeks postpartum, the endometriummay fail to regenerate, leading to Asherman’s syndromeJensen and Stromme.71 Westendorp et al.72 prospectivelyexamined 50 women undergoing either a repeat

Figures 32.8A to C: (A) Three-dimensional USG of the volume of the uterus on day 28 and; (B) Uterine cavity on Day 7

after normal delivery; (C) With 3D power Doppler a localized area of increased vascularity within the myometrium is seen

CHAPTER 32 / Postpartum Ultrasound 527

removal of placental remnants after delivery or a repeat

curettage for incomplete abortion At a later

hystero-scopy, 20 out of 50 (40%) women had intrauterine

adhesions The prevalence of Asherman’s syndrome is

2% after manual evacuation of the placenta but, 37 5%

after postpartum curettage.72 Recently, an update on

intrauterine adhesions has been published and the

importance of prevention has been emphasized.73

First studies concerning RPT performed with old

ultrasound equipment showed high rate of false-positive

diagnosis.4,5,8 Similar results have been obtained by

modern ultrasound equipment.58-68 Published studies

have demonstrated a variable sensitivity (42–94%) and

specificity (62–92%) for ultrasound diagnosis of RPT.

58-68 On the other side, ultrasound appears as a valuable

tool to confirm an empty cavity Lee and Mandrazzo8

found empty cavity in 20 of 27 patients with late

puerperal bleeding In only one case, RPT was confirmed

The same authors reported that histological confirmation

was obtained in eight of nine patients with ultrasound

suspected RPT Although ultrasound technology

improved considerably, the diagnosis of RPT is still

difficult Ultrasound finding of RPT may vary depending

on many different factors We cannot expect the sameultrasound image during early (Figs 32.4A and 32.5A)and late period of the puerperium (Figs 32.4C and 32.5D).The presence of blood, blood clots, necrotic decidua,membranes or gas can give various ultrasound imagesand a proper diagnosis is sometimes difficult.Nevertheless, the most common ultrasound findingassociated with RPT is an echogenic mass8,34-35,55,57-68 (Figs32.9A to C, 32.10A and B, 32.11A and B, 32.12A, 32.13A

to C and 32.14A) In contrast, Edwards et al.15 found inhis study an echogenic mass on day 7 in 51% of normalcases, in 21% on day 14 and in 6% on day 21 Hequestioned ultrasound finding of an echogenic mass inuterine cavity as a sign of RPT However, the definition

of an echogenic mass was not specified and we mayhypothesize that others investigators would probablyclassify many of their “echogenic mass” as

“heterogeneous patterns” A heterogeneous pattern is acommon and insignificant finding of the involutinguterus13 (Figs 32.4B and 32.5C to D) It is located in thecervical area in the early puerperium, in the whole uterinecavity in the middle part of the puerperium and it is notcommon during late postpartum period.13 Sokol et al.16

Figures 32.9A to D: Puerperal abnormalities revealed by ultrasound (A) Retained placental tissue 2 days postpartum;

(B) Blood flow in relation to retained placental tissue; (C) Retained placental tissue 6 weeks postpartum; (D) After curettage

a thin, echogenic endometrium

used the same classification and found “echogenic

material” in 40% of women 48 hours after a normal

delivery However, 14 of the 16 cases demonstrated

echogenic material in the lower uterine segment, while

only two had such findings in the fundus It is unclear if

“echogenic material” is the same as an “echogenic mass”

or if it might be a mixed echo pattern If dysfunctional

postpartum bleeding persists for a long time, RPT is

highly suspected Hertzberg et al.34 described so-called

“stippled pattern” of scattered hyperechogenic foci that

later on became increasingly generalized echogenic,

reflected secondary regressive changes in RPT (Figs 32.9C

and 32.11A)

Two studies61,62 compared the diagnostic accuracy

of clinical assessment with transabdominal USG in themanagement of SPH and concluded that both methodswere of limited value In contrast, recently publishedstudies that assessed diagnostic accuracy of combinedclinical and sonographic protocol, concluded that thecombined approach was accurate and highly sensitivetool for the diagnosis of retained placental tissue.66-69

There are many reasons for discrepancies in thepublished reports Factors that might explain the lowsensitivity and high false-positive rate include a vaguedefinition of the USG diagnosis of RPT,58-62 retrospectivestudy design34,60,64,65 and mixed study populations

Figures 32.10A and B: Puerperal abnormalities revealed by ultrasound (A) Transabdominal transverse scan, 9 days

postpartum, shows retained placental tissue seen as an echogenic mass; (B) A low resistance blood flow is seen on one side

of the echogenic mass

Figures 32.11A and B: (A) Transvaginal longitudinal scan shows retained placental tissue 6 weeks postpartum;

(B) By color Doppler, feeding vessels are seen inside the echogenic mass

CHAPTER 32 / Postpartum Ultrasound 529

including women with bleeding after an abortion and

women with postpartum haemorrhage.8,60,64-66 Three

studies often cited in the published literature evaluated

asymptomatic women.55,58 The accuracy of postpartum

USG for detection of RPT was calculated either from a

small proportion of women who underwent curettage,

assuming that women who had an uneventful puerperal

course after conservative treatments had no RPT,34 60-62

or from histological findings among asymptomatic

women.55,58 Finally, the patients and clinicians have not

been blinded to the sonographic results in any of the

published studies If ultrasound finding shows an empty

cavity with thin white decidua/endometrium during

early (Figs 32.2A and 32.4A) or late puerperium

(Figs 32.4C, 32.5D and 32.6A), pure

fluid/hetero-geneous content in the cavity during the middle part of

the puerperium (Figs 32.4B and 32.5B and C), or only

small echolucent or hyperechogenic dots throughout

whole postpartum period, a clinically significant

amount of retained placental tissue is unlikely.13,34

Transvaginal ultrasound with high frequency probe as

well as transvaginal sonohysterography may better

differentiate intrauterine puerperal pathology.74-77

Doppler Ultrasound During

Pathological Puerperium

A few studies investigated pulsed and color Doppler

during puerperium in order to improve diagnostic

accuracy of ultrasound regarding RPT.60,74,75 Some

investigators observed low resistance blood flow around

intracavitary contents74-78 (Figs 32.9A and 32.10A)

Ashiron et al.74 measured resistance index (RI) in

relation to RPT and found that diagnosis is highly

suspected if RI is below 0.35 (Fig 32.9B) These patients

are suitable for invasive treatment RI above 0.45 should

exclude diagnosis Values between 0.35 and 0.45 form

a “gray zone” (Fig 32.10B) Conservative treatment and

repeated ultrasound examinations should be performed

Power Doppler seems to be a new unexplored

modality that could improve our abilities to diagnose

clinically significant RPT Retained placental tissue in

the uterine cavity might cause a delay in the normal

involution of uterine vessels.40,41 By color Doppler

ultrasound, a localized area of increased vascularity

within the myometrium may be detected.47,78-83 The

presence of a hypervascular area in the myometrium,

within or close to the echogenic mass, has previously

been interpreted alternatively as a common

physio-logical finding,47 as a finding associated with the

presence of RPT60,74,75,83,84 or with arteriovenous (AV)

malformations.25,78,79 Pulsed Doppler usually

demons-trates a low resistance turbulent flow with high systolicvelocity, resembling AV malformations It has recentlybeen suggested that curettage should not be performed

on patients who present with SPH and a color Dopplerimage of a hypervascular area within the myomet-rium.78,79 Van den Bosch80 examined 385 consecutivepostpartum women and reported that a hypervasculararea in the uterus was relatively common (8.3%) anddisappeared either spontaneously or after removal ofplacental remnants Mungen81 has drawn attention to atendency to overdiagnose true AV malformations Hepointed out that a majority of hypervascular areas inthe myometrium probably represented normal “peri-villous flow” in the spiral arteries The regression periodmay be prolonged in the presence of RPT Only in veryrare instances do they represent true arteriovenousmalformations In our recent work on angiographicembolization for treatment of major postpartumhemorrhage, no true AV malformation was diagnosedamong 20 patients but four cases had pseudoaneurysm85

(Figs 32.15A and B)

Our knowledge on uterine artery flow in womenwith RPT is sparse It could be that RPT prevents thephysiological changes in uterine blood flow during thepuerperium The results of our small study83 showedthe resistance flow indices in uterine artery below the10th percentile for 8 of 20 (40.0%) women of which sevenhad histological confirmation of RPT and one did not.There was, however, considerable overlap No patienthad resistance indices above the 90th percentile In 12

of 20 (60.0%) patients, an early diastolic notch wasabsent Early diastolic notches appeared relatively latecompared to the findings in normal population Onlyone woman had a notch before postpartum day 28.Color Doppler showed a hypervascular area close tothe echogenic mass in 12 of 20 (60%) patients, all withhistologically confirmed RPT This figure is slightlyhigher than that reported by Durfee et al.60 (55%) and

by Zalel et al.77 (46%) A hypervascular area was absent

in eight patients (40%) of which six had an echogenicmass that was histologically confirmed RPT Ourfindings that the absence of blood flow does not excludeRPT are in concordance with previously reportedresults.60,77

sound finding in cases of endometritis is the presence

of gas in the uterine cavity.10 Madrazo found gas in

uterine cavity in 15% of patients with puerperal

endo-metritis.10 Nowadays, infections caused by gas-forming

organisms C perfringens are very rare and large

gas-bubbles are almost never seen Moreover, Wachsberg

and Kurtz36 detected gas in about 19% of normal cases,

which is in accordance with results of a computed

tomographic study performed within 24 hours of

uncomplicated vaginal delivery (21%) Ultrasound

appearance of gas is seen as an intensively

hyperecho-genic focus equivalent in echohyperecho-genicity to bowel gas with

clean and dirty shadowing or a reverberation artefact.89

According to our experience, gas is mostly observed

following intrauterine manipulations90 (Figs 32.12B and

32.16A) although it is occasionally observed after

normal vaginal delivery.13 The detection of gas within

the uterine cavity may be a normal finding during the

puerperium and does not necessarily indicate the

presence of endometritis or RPT.13,36 After CS or

Figures 32.12A and B: (A) Transverse longitudinal scan, 11 days postpartum, shows retained placental tissue seen as

an echogenic mass; (B) A thin echogenic endometrium is visible soon after curettage

Figures 32.13A to C: (A) Transabdominal longitudinal scan of the uterus on day 17 postpartum Suspected retained placental

tissue seen as an echogenic mass in the uterine cavity (red arrow); (B) 3D USG shows the volume of the suspected retained placental tissue; (C) Power Doppler angiography, glass body mode shows vessels in the placental tissue (red arrow)

intrauterine manipulations highly echogenic foci canobscure an existing mass in the uterine cavity or bemistaken for retained placental tissue.34,90 Thus when-ever highly echogenic foci are present in the uterinecavity, the physician who interprets ultrasound findingmust be aware of recent uterine manipulations Gasusually disappears within 1–2 weeks after instrumen-tation90 (Fig 32.16B) Furthermore, it has been claimedthat ultrasound image of RPT and endometritisoverlap.8,52 Results from published studies on this issueare inconsistent.8,41,52-53,62,70,90 Pelage et al.91 described

14 cases with uncontrollable SPH undergoing selectiveangiographic embolization Six of 14 patients hadclinical and ultrasound signs of endometritis with RPT

In four cases, histological confirmation was obtained.Two patients had pure endometritis Conversely, Kong

et al.41 pointed out that endometritis appeared to be anoverstated cause of SPH He found that less than 5% ofcases could be ascribed to endometritis Ben-Ami et al.62

found that a majority of the patients presenting with

CHAPTER 32 / Postpartum Ultrasound 531

Figures 32.14A to D: Ultrasound image of placenta praevia perccreta left in situ (A) Color Doppler and; (B) Power Doppler

show the interface between the uterus and urinary bladder 7 days after cesarean section; (C) Retained placenta occupies the most part of the uterine cavity (arrow); (D) Power Doppler shows increased myometrial vascularity behind the retained placenta (arrow)

Figures 32.15A and B: (A) Transabdominal scan of the uterus on day 8 postpartum shows a huge defect in the uterus

forming a pseudoaneurysm (arrow) Color Doppler reveals a feeding damaged uterine artery; (B) Angiography confirmed the ultrasound finding