placenta, imagenes y literatura

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Ultrasound of the Placenta: A Systematic Approach. Part I: Imaging

J.S. Abramowicz a,*, E. Sheiner b

a Department of Obstetrics and Gynecology, Rush University Medical Center, 1653 West Congress Parkway, Chicago IL 60612, USAb Department of Obstetrics and Gynecology, Soroka University Medical Center, Ben Gurion University of the Negev, Beer Sheva, Israel

Accepted 20 December 2007

Abstract

Diagnostic ultrasound has been in use in clinical obstetrics for close to half-a-century. However, in the literature, examination of the placenta

appears to be treated with less attention than the fetus or the pregnant uterus. This is somewhat unexpected, given the obvious major functions

this organ performs during the entire pregnancy. Examination of the placenta plays a foremost role in the assessment of normal and abnormal

pregnancies. A methodical sonographic evaluation of the placenta should include: location, visual estimation of the size (and, if appearing ab-

normal, measurement of thickness and/or volume), implantation, morphology, anatomy, as well as a search for anomalies, such as additional

lobes and tumors. Additional assessment for multiple gestations consists of examining the intervening membranes (if present). The current re-

view considers the various placental characteristics, as they can be evaluated by ultrasound, and the clinical significance of abnormalities of these

features. Numerous and varied pathologies of the placenta can be detected by routine ultrasound. It is incumbent on the clinician performing

obstetrical ultrasound to examine the placenta in details and in a methodical fashion because of the far reaching clinical significance and po-

tentially avoidable severe consequences of many of these abnormalities.

Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: Placenta; Pregnancy; Complications; Fetus; Ultrasound; 3D ultrasound

1. Introduction

Although diagnostic ultrasound has been in use in clinical

obstetrics for close to half-a-century, often, in the literature,

examination of the placenta appears to be treated with less

attention than the fetus or the pregnant uterus. This is some-

what unexpected, given the many important tasks this organ

performs during the entire pregnancy, from fetal oxygenation e

from the earliest stages of gestatione

to nutrition, as wellas tremendous endocrinological influences and protein syn-

thesis in addition to its protective function [1,2]. As has

been shown in multiple journal articles and book chapters

[3e9], examination of the placenta plays a major role in

the assessment of normal and abnormal pregnancies. A me-

thodical sonographic evaluation of the placenta is vital and

should include: location, visual estimation of the size (and,

if appearing abnormal, measurement of thickness and/or

volume), implantation, morphology, anatomy, as well as

a search for anomalies, such as additional lobes and tumors.

Multiple gestations require additional assessment of the in-

tervening membranes (if present). The present article will

consider the various placental characteristics, as they can

be evaluated by ultrasound, and the clinical significance of

abnormalities of these features. Assessment of vascularityis also very important and will be the subject of a subsequent

article.

2. Location

Ultrasound is the ideal tool to determine where the placenta

is implanted. In fact, this was one of the first uses of ultrasound

published in the literature [10,11]. Around 4e5 weeks gesta-

tion (menstrual age), soon after implantation occurs and* Corresponding author.

E-mail address: [email protected] (J.S. Abramowicz).

0143-4004/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.

doi:10.1016/j.placenta.2007.12.006

Available online at www.sciencedirect.com

Placenta 29 (2008) 225e240

mailto:[email protected]

mailto:[email protected]



trophoblast (placenta) development commences, one can dis-

tinguish, by endovaginal ultrasound, a thick, echogenic ring,

distinct from the myometrium and representing the placenta

(Fig. 1). Over the ensuing weeks, differential proliferation

and regression occur to form the definitive placenta [12].

When the placental site is normal (i.e. not at or near the cervical

internal os), most clinicians feel that the exact location (ante-rior, lateral or posterior uterine wall) is not clinically important.

Some, however, have implicated certain (normal) placental

locations with pathological fetal lies such as breech or an in-

crease in occiput posterior presentation with anterior placentas

[13e15]. Implantation in areas with less blood supply, such as

a myoma (Fig. 2). or a uterine septum can be associated with

later complications, such as spontaneous miscarriage [16], in-

trauterine growth restriction, preterm labor, placental abruption

and postpartum hemorrhage [17].

2.1. Placenta previa

This occurs with abnormal implantation of the placenta,

within the lower uterine segment, overlying or proximate to

the internal os of the uterine cervix [9]. It is an important cause

of bleeding during the second half of pregnancy, occurring in

one in 200e250 pregnancies. The classical presentation is

painless bleeding [18]. There are several classifications in the

literature; the most commonly used being: no previa (normal

implantation location), low lying placenta, when the placental

edge is close to the margin of the internal cervical os, generally

2 cm. or less, marginal previa with the placental edge at the

margin of the internal os (hence, occasionally low lying is in-

cluded) and complete previa, with the internal os completelycovered by placental tissue [19,20]. In modern obstetrical prac-

tice, diagnosis is mainly by transvaginal ultrasound, which is

superior to the abdominal approach [19e21]. Most cases of pla-

centa previa are, originally, asymptomatic and are diagnosed

during routine ultrasound investigation. Etiological factors

to consider are previous cesarean sections [22], uterine

transcavitary surgery as well as prior vigorous sharp curettage.

It is also more common in advanced maternal age and multipar-ity [22e25]. Patients with a complete placenta previa need to be

delivered by cesarean section. However, when the distance be-

tween the placenta and the cervical os is greater than 2 cm,

women may safely have a vaginal delivery [19]. Fig. 3a repre-

sents complete placenta previa and Fig. 3b marginal previa.

When the placenta is determined to be previa, an effort should

be made to establish whether abnormal implantation also exists

(see below). ‘‘Placental migration’’ is the term applied to per-

ceived displacement of the placenta from a low or previa im-

plantation to a higher position in the uterus, in relation to the

cervix, as documented by ultrasound [24,26,27]. An example

is demonstrated in Fig. 4. Most believe there is not truly a mo-

tion of the placenta, but rather a process involving peripheral

degeneration secondary to decreased vascularization with pref-

erential growth in areas assumed to be optimally perfused [28].

Another, perhaps more plausible, explanation is proportionally

more rapid growth of the lower uterine segment, as compared to

the rest of the uterine body. In fact, both theories may act in con-

junction. Whichever is the exact explanation, close examination

of placental position is important in predicting mode of delivery

[24,29].

When the placenta is low lying or marginal in the second

trimester, a potential later complication, particularly if ‘‘migra-

tion’’ occurs is vasa previa. While not a form of placenta previa,

vasa previa is somewhat related and an important clinical entityto keep in mind, with potential catastrophic results and will thus

be discussed here.

2.2. Vasa previa

This rare condition, with likely preventable, severe compli-

cations carries a risk of fetal exsanguination and death when the

membranes rupture [30e33]. This is due to the fact that fetal

vessels run through the membranes, unprotected by placental

tissue or Wharton’s jelly, below the fetal presenting part and

close to the internal cervical os. It should particularly be sus-

pected when the placental edge covers the os in mid-pregnancy

Fig. 2. Placental implantation on a submucosal myoma. Severe IUGR was

diagnosed around 26 weeks.

Fig. 1. Placenta (trophoblast) at 6 weeks gestation, endovaginal scan. Note the

echogenic (white) ring surrounding the gestational sac (black circle), repre-

senting the early placenta. The fetus is marked by arrowheads.

226 J.S. Abramowicz, E. Sheiner / Placenta 29 (2008) 225e 240



but recedes later on (see above). Risk factors include multiple

pregnancy, pregnancy resulting from IFV, presence of velamen-

tous insertion of the umbilical cord, succenturiate or accessory

placental lobes. Velamentous insertion of the cord refers to

vessels traveling through the fetal membranes before entering

the actual placenta, as opposed to the normal insertion of the

cord directly into the placenta. This has to be differentiated

from marginal insertion of the cord, when the insertion is at

the placental edge, rather than more centrally (Fig. 5). Vasa

previa can be diagnosed prenatally by ultrasound examination(Fig. 6a). It should be distinguished from funic presentation,

when loops of a normally implanted cord are preceding the pre-

senting part at the internal os (Fig. 6b). With funic presentation,

manual displacement of the presenting part and manipulation of

the lower segment, generally demonstrate movement of the

loops of cord [34]. This will not occur in vasa previa. A recent

report suggests that a high ultrasound detection rate for vasa

previa is achievable [35]. The authors concluded that the prena-

tal diagnosis of all cases of vasa previa achieved during the sec-

ond-trimester scan allowed them to avoid any prenatal death

related to this condition [35]. Three-dimensional sonography

and power angiography can also add to the prenatal diagnosis

of this condition [33]. Favorable outcome depends on prenatal

diagnosis and cesarean delivery at 35 weeks or before the mem-

branes rupture [30,31,33].

3. Anomalies of implantation

Normal implantation occurs with the bastocyst eroding

through the endometrial epithelium into the subepithelial con-

nective tissue. Its progression to deeper layers is interrupted by

the formation of an essentially acellular fibrinoid layer, known

as Nitabuch’s layer or stria.

3.1. Placenta accreta

The condition is defined as abnormal adherence of the pla-

centa to the uterus, probably due to an absence or deficiency of

Nitabuch’s layer or the spongious layer of the decidua [20,36].

Invasion to the myometrium is defined as placenta increta

(Fig. 7a), and invasion through the myometrium and serosa

is called placenta percreta [20] (Fig. 7b). The incidence of

placenta accreta is rising, primarily because of the rise in

Fig. 4. Placental ‘‘migration’’. (a) the posterior placenta is at the level of theinternal os at 23 weeks gestation (arrowheads); (b) the placental edge is

now 1.85 cm from the internal os, at 28 weeks gestation.

Fig. 3. Placental location, endovaginal scan. (a) Complete placenta previa.Cervix is marked by arrowheads; (b) marginal placenta. Cervix is marked

by arrowheads and placental edge is 0.47 cm from the internal os.




cesarean deliveries [20,36]. The risks increase with the num-

ber of previous cesarean section [37]: 4-fold after one previous

cesarean section, up to 11.3 relative risk increase after two.

Furthermore, patients with a previous cesarean section and

previa implantation of the placenta are five times more likely

to have placenta accreta. Another etiological factor is local

tissue alteration, secondary to curettage. The condition can

be associated with massive blood loss at delivery. Ultrasound

imaging is widely used for the screening of placenta location

and potential abnormal development [20,36,38,39]. This exam

is associated with high sensitivity and specificity for diagnosis

of placenta accreta when specific defined criteria are used for

the diagnosis. Prenatal diagnosis of placenta accreta by

imaging should be based on the irregularly shaped placental

lacunae signs (‘‘Swiss cheese’’ appearance) representing vas-

cular spaces (Fig. 7a) rather than only the loss of the normally

obvious retroplacental clear space [19,20,39,40]. Other signs

include thinning of the myometrium overlying the placenta,

protrusion of the placenta into the bladder, increased vascular-

ity of the uterine serosaebladder interface, and turbulent flow

through the lacunae using Doppler studies [4,19,20,36,41]. An

analysis of the different sonographic criteria [42] demon-

strated a very high sensitivity for the presence of lacunae

(93% with 93% positive predictive value [PPV]), followed

by obliteration of the clear space at the placentalemyometrial

junction (only 7% sensitivity and 6% PPV but increasing to

Fig. 5. Marginal insertion of the cord. (a) The cord inserts at the margin of the

placenta (arrowheads) and runs in the membranes for a short distance (double

arrowheads), hence velamentous. (b) Power Doppler imaging demonstrates

insertion of the cord at the lower edge of the placenta. (c) In this 3D recon-

struction, the cord insertion (arrowheads) is at the placental edge.

Fig. 6. Vasa previa vs funic presentation. (a) Twin pregnancy. Color Dopplerdemonstrates fetal vessels (Twin A) at the level of the internal os. No displace-

ment occurs with abdominal palpation. This is consistent with vasa previa.

(b) Note several loops of cord at the level of the internal os. With palpation,

these loops are mobile. This represents funic presentation.




73% sensitivity and 85% PPV when considered with another

criterion) and last, obliteration of the posterior bladdere

uterine wall interface (20% sensitivity and 75% PPV). The

lacunae and their significance could be documented in over

80% of cases from 15 weeks gestation, on [42]. Placental

MRI was, originally, expected to be a superb tool for the diag-

nosis and morphological description of placenta accreta but

was found not as useful as expected. However, more recent

publications have demonstrated topographical information

that optimizes diagnosis and surgical management [43e45].

While ultrasound remains the main, and often the only neces-

sary, diagnostic tool, in some situations screening of placenta

accreta could be improved with the use of a combination of

these diagnostic techniques (ultrasonography first, and then

MRI for cases with inconclusive ultrasound features), and

benefit high-risk populations with a reduction in morbidity.

Following prenatal diagnosis, planned peripartum manage-

ment by a multidisciplinary team, may help reduce morbidity

and mortality. The majority of women with significant degrees

of placenta accreta will require a hysterectomy although

a successful conservative management has also been described

[20,45].

3.2. Abruptio placentae (placental abruption)

This is defined as premature separation of a previously nor-

mally implanted placenta. This is a leading cause of vaginalbleeding in the latter half of pregnancy, complicating about

0.5e1% of pregnancies [46,47]. Nevertheless, in preterm

deliveries this complication can reach an incidence of 5%

[48]. Risk factors are defined and consist of abruption in

a previous pregnancy (by far the strongest factor), maternal

hypertension (found in over 40% cases), advanced maternal

age, smoking, cocaine use, trauma and some uterine anomalies

[47,49]. In addition, abruption may take place in the presence of

rupture of the membranes [50,51]. Most cases of placental

abruption cannot be predicted or prevented [47]. Abruption is

an important cause of perinatal mortality and morbidity. In

a large population-based study, placental abruption was found

as the strongest cause for perinatal mortality, with an odds ratio

of 50.5 [48]. The diagnosis of abruption is a clinical one, and

ultrasonography is of limited value with a sensitivity of no

more than 50% [46,47]. On ultrasound one might see placental

edge separation, subchorionic and retroplacental hematomas.

In the acute phase, the area of detachment may appear hypere-

choic, becoming hypoechoic after a few days. Because of

a somewhat similar sonographic appearance by uterine

contractions, myomata or vascular plexuses, ultrasound is not

sensitive for detection of placental abruption, but a positive

finding is associated with more aggressive management and

worse neonatal outcome [46]. The management of abruption

should be individualized on a case-by-case basis dependingon the severity of the abruption and the gestational age at which

it occurs.

3.3. Placental bed infarction

Also known as intervillous thrombosis, this is a vascular le-

sion caused by thrombosis in the villous spaces [52]. It appears

as round, mostly anechoic, intraplacental, measuring up to

several centimeters. It is common and, unless massive, which

is very rare, of minimal clinical significance. It may, however,

point to some communication between the fetal and maternal

circulations and, as such, may have a role in cases of sensiti-zation. It is different from maternal floor infarction (not a true

infarct), a recurrent lesion of unknown etiology, in which

fibrin is deposited throughout the placenta, leading to necrosis

of villi, and often accompanied by fetal demise [53].

3.4. Hematomas1

Abnormal collections of blood are frequently observed

while performing obstetrical ultrasound [54e57]. They appear

Fig. 7. Placenta accreta. (a) Increta: the placenta penetrates through themyometrium. Note thin echofree line (arrowheads), demonstrating placentale

myometrial boarder in the upper part of the image but disappearing, close to

the lower arrowhead, as well as cystic areas (‘‘swiss cheese appearance’’).

(b) Percreta: the placenta reaches the bladder wall and infiltrates the anterior

cervical lip. Patient complained of hematuria.

1 The correct grammatical plural of hematoma is hematomata but hemato-

mas is the more commonly used form.




as crescent-shaped, sonolucent fluid. These can be on the fetal

(preplacental, aka retrochorionic, aka subchorionic) or mater-

nal (retroplacental) side [57]. Confusion occasionally exists

in the literature because the placenta is thought of as the cho-

rion; hence retroplacental hematomas are sometimes referred

to as retrochorionic. Furthermore, there is another entity where

blood is found near the umbilical cord insertion, often resultingfrom pulling on the cord, limited by the amniotic membrane

and designed as subamniotic hematomas (see below). Retro-

chorionic hematomas are lesions involving maternal blood

separating the chorionic membrane from the villous chorion

(Fig. 8). They are, generally, of minimal clinical significance,

except if accompanied by clinical symptoms, such as vaginal

bleeding or uterine contractions when they can be markers of

later complications, such as abortion, IUGR, preterm labor,

placental abruption and fetal distress [57,58]. A particular,

rare, form is called Breus mole, when the hematoma is massive

and is associated with IUGR and/or fetal demise [59]. If ob-

served with grey-scale only, they are commonly confused

with chorioangioma [60]. However, blood flow is absent inhematomas, when power or color Doppler is applied. [58]. Sub-

amniotic hematomas are different. They are situated between

the amniotic and chorionic membrane and result from rupture

of chorionic vessels, near the cord insertion. Hence they are

often a postnatal finding, seen as a result of pulling on the um-

bilical cord during delivery. Prenatal diagnosis occurs occa-

sionally, however [54]. Clinically more significant,

retroplacental hematomas are typically located between the

placental basal plate and the uterine wall (Fig. 9). They usually

bulge towards the fetal side and result from bleeding from the

spiral arteries. They too have been associated with perinatal

complications, particularly preterm labor, perhaps as a resultof uterine irritation, secondary to the presence of blood [57].

The phenomenon is identical to abruption, although often

asymptomatic and self-limited. Clinical management of these

hematomas consists mainly of close observation, although

some recommend bed rest but with no clear evidence of benefit.

Some authors recommend prophylactic therapy with tocolytics,

particularly progesterone.

4. Placental thickness/size (volume)

It has long been known that a relation exists between birth

weight and placental sizes. However, limited information is

available regarding placental volume during pregnancy [61].

Placental size has been shown to be an important factor in ab-

normal fetal growth [62,63]. This relation already exists in the

first trimester, as demonstrated by 3D volume calculations

[64e67]. Although tables exist for thickness of the placenta

as function of gestational age [68], in daily clinical practice,

it is not routine to measure placental thickness. Normal thick-

ness is approximately 2e4 cm, at a central point or near the

cord insertion, when the cord is centrally inserted [7], as seenin Fig. 10a. During examination of the placenta, thickness is

grossly evaluated and, if appearing normal to the eye, is not fur-

ther delineated. Only if suspicious, will the maximal vertical

thickness be measured. Increased thickness is non-specific

and can be found with maternal diabetes, maternal anemia,

abnormalities of fetal growth, fetal hydropse whether immune

or non-immune [69] e and, particularly, in several infections

such as syphilis, cytomegalovirus and toxoplasmosis [70e

72]. Fig. 10b is an example of thick placenta in a case of

non-immune hydrops, secondary to fetal cardiac arrhythmia.

In addition, conflicting reports exist on whether the placenta

is larger or smaller in fetuses with karyotypic anomalies

[6,73e

75]. These do not include cases of coexistence of a fetus

with gestational trophoblastic disease [73e84].

Placental mesenchymal dysplasia is a rare placental vascu-

lar anomaly. Because one of the major morphological compo-

nents is thickened placenta, it will be considered here,

although the main differential diagnosis is with molar degen-

eration (see below). It is characterized by placentomegaly

with the presence of intraplacental anechoic vesicles, resem-

bling partial mole [85e87]. Histologically, no trophoblast pro-

liferation is present (as opposed to molar degeneration and the

major clinical difference with molar pregnancy is that it can

coexist with a normal fetus. However, it has also often been

described in the presence of abnormal karyotypes [88] andFig. 8. Retrochorionic hematoma (arrowheads). This is on the fetal side.

Fig. 9. Retroplacental hematoma (arrows). This is on the maternal side.




specifically with BeckwitheWiedemann syndrome, a fetal

congenital abnormality, characterized by macrosomia, viscer-

omegaly (macroglossia), omphalocele, facial hemihypertro-

phy, hyperinsulinemic hypoglycemia at birth and increased

susceptibility to childhood tumors [85,86]. Among cases with-

out BeckwitheWiedemann syndrome, 50% of fetuses demon-

strated intrauterine growth restriction and/or intrauterine fetaldemise [86,89].

5. Anomalies of placental shape

5.1. Extrachorial placenta: Circumvallate

and circummarginal placenta

When the chorionic plate is smaller than the basal plate of

the placenta, the placental periphery is not covered, leading to

some of the placenta to be extrachorial. Circumvallate and

circummarginal placentae are manifestations of this condition.

Circumvallate placenta (Fig. 11a and b) is caused when the

fetal surface presents a central depression surrounded by

a thickened ring, composed of a double fold of amnion and

chorion with degenerated decidua and fibrin in between, cre-

ating an irregular edge with uplifted margins or placental

Fig. 11. a) Circumvallate placenta. Irregular placental appearance with uplifted

edges (arrow) secondary to the chorionic plate being smaller than the basal

plate. Sonolucencies are present (arrowhead). (b) Diagram of circumvallate

and (c) circummarginal placenta. In both diagrams the limits of the basal

plates are marked with arrowheads and the limits of the chorionic plate with

asterisks.

Fig. 10. Placental thickness. (a) Normal thickness (2.6 cm), measured at theinsertion of the cord, 18weeks GA. Calipers delineate the placenta. (b) Thick

placenta (6.2 cm), in a case of fetal non-immune hydrops, 24 weeks GA. Cal-

ipers delineate the placenta.




sheet or shelf [90,91]. This condition has been linked to pla-

cental abruption, fetal hemorrhage and accordingly to adverse

perinatal outcome, including increased fetal morbidity and

mortality [91]. However, when the ring is flat, rather than

and lacks central depression, it is called circummarginal

placenta (Fig. 11c), a condition with questionable clinical

significance. The accuracy of sonography of the placenta forrevealing circumvallation appears to be limited. Key features

include a ring-like infolding of the fetal membrane upon the

fetal surface of the placenta [92]. Nevertheless, focused pla-

cental sonograms for detection of morphologic abnormality

using the published criteria for circumvallate placenta (irreg-

ular edge, uplifted margin, or placental sheet or shelf) failed

to detect the placental edge abnormality in most cases of

circumvallation [91].

5.2. Accessory lobe: succenturiate placenta

The succenturiate placenta is a morphological abnormalityincluding one or more small accessory lobes that develop at

a distance from the main placenta [93]. It is actually a smaller

version of a bilobate placenta which occurs when two

approximately equal lobes of placenta are found [94,95].

The antenatal recognition of this condition is important since

intramembranous vessels connecting the main placenta with

the succenturiate placenta may rupture during labor with rup-

ture of the membranes (see vasa previa above) and fetal death

may ensue. In addition, retention of this accessory lobe may

lead to postpartum hemorrhage. Using a multivariate analysis,

Baulies et al. found bilobate or succenturiate placenta as an in-

dependent risk factor for vasa previa, with an odds ratio of 22.1[35]. A further rare variant, as far as we know, not yet de-

scribed by ultrasound is the girdle placenta [95]. The placenta

is annular or horse-shoe shaped. It has been associated with

antepartum bleeding and/or IUGR [95].

5.3. Placenta membranacea

Placenta membranacea, or diffused placenta is a condition

in which all of the fetal membranes are covered by functioning

villi. It is a rare form with an incidence of 1:20,000e40,000

[96]. The placenta develops as a thin membranous structure

occupying the entire periphery of the chorion. Part of the pla-

centa is therefore previa, with all its significance. Furthermore,

a large part of the placenta is non-functional from a fetal

maternal exchange standpoint. This rare placental anomaly

can be detected by ultrasound demonstrating a gestational

sac completely covered with placental tissue [97]. Antepartum

and postpartum hemorrhages are reported to complicate 83%

and 50% of the cases, respectively, and approximately 30%

of the cases involve some form of abnormal placental adher-

ence [96]. Partial placenta membranacea is encountered

more frequently than the total or near-total form, but is simi-

larly associated with recurrent antepartum hemorrhage, mis-

carriage or preterm delivery [98].

6. Placental grading

Ultrasonically detectable placental changes are correlated

with fetal maturity, and the placenta is known to mature and

calcify as pregnancy progresses [99]. Significant placental

calcifications are rarely seen before 37 weeks gestation [99].

At 40 weeks gestation or beyond, about 20% of placentashave extensive calcifications. Close correlation between sono-

graphic appearance of the placental texture (grading) and fetal

maturity has been described by several authors [99e101]. The

classification, mostly historical nowadays, as developed by

Grannum et al. [100] consisted of four grades (0e3): with

grade 0, generally seen from early gestation till early 2nd

trimester,with the echogenicity being homogeneous and the

chorionic plate without indentations (Fig. 12a) to grade 3,

from late term (38e39 weeks) and later (post dates) with large,

irregular calcifications with shadowing and indentations of

the chorionic plate penetrating through to the basilar plate

and delineating placental cotyledons (Fig. 12b). The presence

of grade 3, early in pregnancy, was described as signifying

Fig. 12. Placental grading. (a) Grade 0 at 20 weeks gestation. Note homoge-

neous appearance. (b) Grade 3 at 32 weeks gestation, preeclamptic, smoker.

Note interlobar calcification, reaching the basal plate and delineating separate

lobes (arrowheads).




placental dysmaturity, as associated with IUGR and/or smok-

ing, chronic hypertension, SLE, diabetes and other vascular

diseases [100]. While it seems to be clinically valid that prema-

ture aging (grade 3 before 37 weeks gestation) is associated

with more perinatal complications [102], many authors have

shown a lack of direct correlation with IUGR for instance

[103], nor was it found useful to predict postmaturity and fetaldistress [99]. In general its value in low-risk pregnancies was

limited [104] and its reproducibility in question [105]. It is ap-

parent, however, that advanced and premature maturation is

seen in smokers [106,107]. Nevertheless, recently, McKenna

et al. [108] determined the significance of an inappropriately

mature calcified placenta on ultrasound examination. They

concluded that ultrasound detection of a grade 3 placenta at

36 weeks’ gestation might help to identify the ‘‘at-risk’’ preg-

nancy, in terms of subsequent development of gestational hy-

pertension and delivery of a growth-restricted neonate.

7. Placental calcifications

This is considered by some as different from the above and

consists of relatively small echogenic speckles dispersed

through large areas of the placenta [109]. Placental calcifica-

tion usually increases with gestational age and is actually rec-

ognized as a normal part of maturation and aging of this organ

[109]. According to Poggi et al. [110], the mechanism of ap-

atite mineralization probably involves one of three known

mechanisms of tissue calcification: physiological (like bone),

dystrophic (ischemia-related) or metastasis (mineralization in

a supersaturated environment). These calcifications have,

occasionally, been described as areas of ‘‘hyperdensity’’ in

several infectious processes, toxoplasmosis, in particular[70]. Numerous small, echogenic nodules on the fetal surface

may be consistent with amnion nodosum or squamous meta-

plasia. Amnion nodosum is a localized, diffuse accumulation

of amorphous material (vernix caseosa, desquamated fetal

skin cells, fibrillar eosinophilic material, squamous epithelial

cells, and hair) producing small nodules on the placental

surface. It is typically associated with fetal renal agenesis,

hence oligohydramnios and poor fetal outcome. Squamous

metaplasia is similar, localized more around the umbilical

cord insertion. It appears to have no clinical significance. To

our knowledge, neither has been described by ultrasound.

8. Placental tumors

These consist of gestational trophoblastic tumors, nontro-

phoblastic tumors and metastases from cancers in other parts

of the body. In addition, several macroscopic lesions, such

as subchorionic fibrin deposits and intervillous thrombosis,

as well as placental cysts can often be observed.

8.1. Gestational trophoblastic disease (GTD)

This refers to a wide spectrum of proliferative disorders of

the placental trophoblast [111,112]. There is benign (80%)

and malignant trophoblastic disease. Increased beta human

chorionic gonadotropin (b-hCG) secretion characterizes this

condition which is highly curable even in the presence of me-

tastases. The major risk factors for gestational trophoblastic

disease are Asian ethnicity, advanced maternal age and a past

history of gestational trophoblastic disease. Ultrasound is

essential for the identification of GTD [113e115]. Common ul-

trasound presentations include enlarged uterus and absence of fetal parts. Early ultrasound descriptions of the placental tissue

were linked to the appearance of ‘‘snowstorm’’ without embry-

onic structure (Fig. 13). Maternal lakes resulting from stasis of

blood between the molar villi are common as well. Color and

spectral Doppler are important elements of the sonographic

diagnosis [116]. Large ovarian thecaelutein cysts, secondary

to the elevated b-hCG levels may also occur. Since this group

of disorders is one of the highly curable neoplasms, early diag-

nosis and prompt treatment is necessary [112]. Most complete

moles are secondary to diandric duplication (duplication of

paternal chromosomes) and this condition accounts for most

cases of malignant transformation or persistent trophoblastic

disease after partial mole [83]. The partial hydatidiform moleis a histopathologic entity characterized by focal trophoblastic

hyperplasia with villous hydrops together with identifiable fetal

tissue [76e81,84,117]. This results from fertilization of a nor-

mal oocyte by more than a single sperm or a diploic sperm or

fertilization of a diploic oocyte by a normal haploid sperm, all

resulting in a conceptus with three sets of chromosomes

(69XXX or 69XXY). More than 90% of triploid fetuses show

severe, symmetrical growth restriction and multiple structural

anomalies, commonly accompanied by oligohydramnios and

abnormal placental Doppler indices [83]. The typical placental

molar features are not always present in triploid partial moles

and are less likely to be apparent on ultrasound in earlypregnancy [83]. Women with this complication should be

offered pregnancy termination and a careful follow-up. Malig-

nant trophoblastic disease occurs in approximately 15e20% of

patients with hydatidiform mole but rarely in partial mole. On

ultrasound, malignant trophoblastic disease has been described

Fig. 13. Gestational trophoblastic disease. Note diffuse differences in echoge-

nicity, secondary to edema and cystic changes (arrowheads), previously de-

scribed as ‘‘snowstorm’’ appearance.




as irregular echogenic lesions within the myometrium, often

surrounded by echofree areas, corresponding to local hemor-

rhage [113e115].

8.2. Nontrophoblastic placental tumors

Chorioangioma is the most common benign nontrophoblas-tic placental neoplasm [118]. It is a hypervascular cystic lesion,

usually single, but occasionally multiple, with arterial and

venous flow that produces color signals and is often described

in the literature [60,119e133]. Its sonographic appearance

includes a well-circumscribed, rounded, basically hypoechoic

lesion next to the chorionic surface (Fig. 14), often close to

the cord insertion [134]. Diagnosis may not always be simple,

since other lesions, such as hemorrhages may have a similar ap-

pearance [60]. Small lesions are often present when examining

the placentas of completely asymptomatic, normal pregnancies

[118]. Larger lesions (>5 cm) are rare but can be associated

with fetal morbidity (non-immune hydrops, IUGR, neonatal

cardiomegaly, anemia and thrombocytopenia) and mortality

[121e123], as well as maternal morbidity such as polyhydram-

nios and pre-eclampsia [134]. Color Doppler US is useful in the

early diagnosis and differentiation from hematomas [135,136]

as well as evaluation of response to treatment, since blood

flow is prominent in these lesions [137]. Three-dimensional

ultrasound may be used for better visualization of continuity

and curvature of structures [137,138]. In the case of chorioan-

gioma, the thick and rough surface of the tumor can be clearly

depicted [139]. In fact, it appears 3D sonography provides

a novel means of visualizing placental abnormalities in utero

[138]. Placental teratoma is a very rare lesion with only few re-

ported cases [140e

142]. Other cystic lesions can often be seenin the placenta with no relation to neoplastic growth. Most of-

ten, these are collections of blood in maternal vessels, known

as placental lakes (Fig. 15). Most common location is beneath

the chorionic plate [143e145]. Occasionally flow can be

demonstrated with Doppler technology. These lesions are not

known to be associated with clinical pathology [144,145], ex-

cept when found with placenta accreta, in which cases they

are generally identified as lacunae (see above).

8.3. Metastases

Metastasis of maternal malignant tumor to the placenta is

a rare event. Melanoma is the most common maternal malig-

nant tumor to metastasize to the placenta, and it accounts for

one-third of the cases [146]. Another third is divided between

hematological malignancies, such as leukemia and lymphoma

and lung cancers [147]. Breast cancer accounts for 13% of ma-

lignancies, while the remaining is distributed among various

carcinomas and sarcomas [147]. Rarely, the metastases will

reach the fetus and have clinical significance. Even rarer are

metastases from cancer of fetal origin. Such masses can be

visualized prenatally by ultrasound. In all cases of maternal

malignancy, histological examination of the placental shouldbe performed [148] and if metastatic tumor is detected in

the placenta, close follow-up of the baby is obligatory. Placen-

tal abscess is a very rare condition, most commonly secondary

to Listeriosis, that can be mistaken, on ultrasound, for intrapla-

cental metastasis [149].

8.4. Placental macroscopic lesions

Several, mostly cystic, lesions can be observed while scan-

ning the placenta, particularly in more advanced stages of

gestation (late second/third trimesters). They look somewhat

similar to and should not be confused with chorioangioma,

since, as opposed to chorioangioma, they are, generally, of

minimal, if any, clinical significance. Slow flowing maternal

blood may allow for accumulation of fibrin in the area imme-

diately beneath the chorionic membrane (subchorionic fibrin

deposition). This is clinically not significant [12]. Intervillous

thrombosis is due to maternalefetal hemorrhage, when fetal

blood escapes vessels and mixes with maternal blood in

villous lakes. Clinical significance is unclear, although it

may play a role in Rh isoimmunization (see above, Placental

Bed Infarction).

Placental cyst is a rare, mostly benign [150], subchorionic

lesion, filled with mucoid material (Fig. 16). It is a single find-

ing in most cases, but, occasionally, multiple cysts are present.

Fig. 15. Placental lake (yellow arrows). Note proximity to maternal vessel

(arrowheads).

Fig. 14. Chorioangioma (arrowheads).




Only if large (>4.5 cm) have they been associated with fetal

complications, such as IUGR [151] or fetal demise [152,153]

although even very large ones have also been described with

no consequence to the fetus [154]. Table 1 offers a summaryof the salient sonographic and clinical features of these lesions.

9. Placenta in multiple gestations

All twin pregnancies are at high risk for perinatal morbid-

ity and mortality compared with singleton gestations. The

major threats to perinatal survival in twin gestations are pre-

term delivery and the clinical complications of monochorio-

nicity [155]. Monochorionic twins originate from one ovum,

fertilized by one sperm cell, which subsequently divides

(monozygotic, aka identical twins). Time of division, after

fertilization will determine whether monozygotic twins will

be dichorionicediamniotic (days 1e3), monochorionice

diamniotic (days 3e8), monochorionicemonoamniotic (days

8e

10) or conjoint (after day 12) [7]. Two ova, fertilized bytwo sperm cells yield dizygotic (aka ‘‘fraternal’’) twins and,

as a rule, will always be dichorionicediamniotic. Monochor-

ionic placentation occurs in approximately 25% cases of twin

gestations. The monochorionic (MC) placenta is appropriate

for a singleton fetus, and therefore may not be sufficient for

twins [156]. In addition, monochorionic twins are at further

risk for type-specific perinatal complications, for example,

twinetwin transfusion syndrome (TTTS) [156]. Problems

may arise from asymmetric cord insertions. Indeed, there is

a higher frequency of velamentous and marginal cord inser-

tion in twins, potentially leading to growth discordance as

Fig. 16. Placental cyst, multiplanar and 3D volume (arrowheads).

Table 1

Placental non-malignant macroscopic lesions

Location Appearance Size Blood flow Clinical Significance

Chorioangioma Next to chorionic

surface

Heterogeneous, anechoic

but may contain mildly

echogenic material (mucus)

Variable Hypervascular If >5 cm, risk of NIH, IUGR,

anemia, IUFD

Lakes Beneath chorionic

plate

Echofree (maternal vessels),

appearance may change

Variable Occasional,

turbulent, slow

None, except if associated

with placenta accrete (see text)

Subchorionic fibrin

deposition

Subchorionic Echogenic Variable,

usually small

No None

Intervillous thrombosis Intraplacental Round, usually anechoic Variable,

usually small

No None, perhaps role in

isoimmunization

Cyst Subchorionic Echofree Variable No If >4.5cm, risk of IUGR, IUFD

Abbreviations: NIH: non-immune hydrops, IUGR: intrauterine growth restriction, IUFD: intrauterine fetal demise.




a result of unequal sharing of placental tissue [157]. It is

estimated that 95% of MC twin placentas contain interfetal

vascular connections [158]. These connections may be indi-

rect artery-to-vein (AeV), found in up to 80% cases, within

the placental villi, direct artery-to-artery (AeA), in 75%, at

the fetal surface, or direct vein-to-vein (VeV) in 20%, also

at the fetal surface. The Ae

V connections are responsiblefor TTTS, when unidirectional while AeA may protect

against it but lead to twin reversed arterial perfusion

(TRAP), together with VeV connections. In TRAP sequence,

one twin (‘‘pump’’ twin) forces blood to the entire placenta

and the acardiac twin who acts as an additional cotyledon

but without reoxygenating that amount of blood that passed

through it. The pump twin may suffer damage as a result.

In addition, sluggish flow increases risk of thrombosis and

thromboembolic phenomena in the pump twin. Additionally,

if one twin dies, from selective termination or spontaneously,

the survivor is also at risk of suffer damage [156], neurolog-

ical, in particular as well as disseminated intravascular coag-

ulation, secondary to dissemination of coagulation factorsfrom the deceased twin to the live one. Cord entanglement

is another risk, specific to monoamniotic twins, as is, often,

discordancy for congenital anomalies [156]. As a result, in-

creased fetal surveillance has been advocated for twins. Ultra-

sound has made a dramatic impact on the obstetric

management of complicated twin pregnancies [156]. In par-

ticular, technological advances in ultrasound have contributed

to improvements in prenatal diagnosis. Transvaginal scanning

has allowed better resolution and improved structural charac-

terization and chorionicity. Growth concordance is considered

a reassuring sign in twins. Conversely, discordance (>20e

25% estimated weight difference) is thought to possibly re-flect a hostile intrauterine environment at least to the smaller

twin. Consequently, increased surveillance of discordant

twins is common practice. With the realization that perinatal

morbidity and mortality are higher in monochorionic than

dichorionic twins, attempts have been made to assign chorio-

nicity by ultrasound [156,159e161]. Precise first-trimester

depiction of chorionicity has enabled early antepartum strati-

fication of twin gestations according to chorionicity, using the

number of placental masses, fetal gender, septal thickness and

the ‘‘twin peak’’ sign. Assessment of chorionicity is best per-

formed in the first trimester when accuracy approaches 100%

before 14 weeks [161], but even in the third trimester, using

a composite cascade of available sonographic features, accu-

racy has been reported to approach 97% [155]. The identifi-

cation of different fetal gender or the clear separation of

two placentae at any gestational age indicates dichorionic

twinning. Nevertheless, in most twin pregnancies other fea-

tures need to be assessed to determine chorionicity. When

a single placental mass is identified, it may be difficult to dis-

tinguish whether there is one placenta or two fused placentas.

The ‘lambda’ or the ‘twin peak’ sign refers to the triangular

projection of tissue extending up to the base of the inter-

twin membrane in dichorionic placentation [7], first described

in 1992 [159] (Fig. 17a). It is based on the presence of echo-

dense chorionic villi between the two layers of chorion at its

origin from the placenta. This sign reflects persistence of the

chorion frondosum [155,162]. However, as the pregnancy ad-

vances into the second and third trimesters, regression of the

chorion frondosum to form chorion laeve means that the twin

peak sign cannot be reliably used to determine chorionicity.

Usually, membrane configuration in a monochorionic preg-

nancy has been described with the ‘T’ sign, where the mem-brane approaches the placenta at around a 90 angle

(Fig. 17b) [155]. The inter-twin membrane thickness mea-

sured by ultrasound is greater in dichorionic twins because

of the greater number of layers present. The presence of

a thick, i.e. greater than 2 mm dividing membrane, from 10

to 14 weeks, supports the diagnosis of dichorionicity [163].

Importantly, it is best at determining chorionicity at the ex-

tremes of measurement, with difficulty in diagnosis around

the ‘cut-off’ zone [164]. The presence of the ‘lambda’ or

the ‘T’ sign in the presence of a single placenta, best deter-

mined in the first trimester, is the most reliable indicator of

chorionicity, with measurements of the inter-twin membrane

thickness and counting of the membrane layers being lessreliable [160]. This analysis of the membranes should be per-

formed in higher rate multiple gestations in a similar fashion

(Fig. 18). Doppler techniques allow accurate flow studies of

Fig. 17. Inter-twin membranes in diamniotic twins. (a) ‘‘Twin peak’’ in dichor-

ionic twins (arrowheads). (b) ‘‘T sign’’ in monochorionic twins (arrows).




vessels in the placenta and fetus and can contribute to the

management of discordant twins, for intrauterine growth re-

striction, fetal anemia and twinetwin transfusion syndrome.

Three-D ultrasound may add to the accuracy of diagnosis

[165,166], although its role has not yet been determined.

10. Conclusions

As evidenced by this review, numerous and varied patholo-

gies of the placenta can be detected by routine ultrasound. It

is incumbent on the clinician performing obstetrical ultrasound

to examine the placenta in details and in a methodical fashion

because of the far reaching clinical significance and potentially

avoidable severe consequences of many of these abnormalities.

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