Sonographic Imaging of Maternal Complications of Pregnancy Image Presentation

Image Presentation
Sonographic Imaging of
Maternal Complications
of Pregnancy
Donald N. Di Salvo, MD
Objective. To show the role of diagnostic sonography in delineating pathologic conditions occurring
during and immediately after pregnancy. Methods. Cases illustrative of a broad range of pathologic
conditions were collected primarily from personal experience in a busy ultrasound clinic serving highand low-risk pregnancies over the past 15 years, with supplemental cases drawn from departmental
teaching files. Sonography was the primary diagnostic tool, with confirmation obtained from other
imaging modalities in select instances. Results. Cases were organized on an anatomic and time-ofonset basis. For conditions occurring during pregnancy, the following anatomic areas are considered:
the liver and biliary tree, urinary tract, bowel, ovary, and uterus and placenta. For postpartum complications, the following conditions are discussed: subfascial and bladder flap hematomas, retained products of conception, and ovarian vein thrombophlebitis. Although the main imaging modality in these
conditions was sonography, correlation with computed tomography and magnetic resonance imaging was also made in several cases. Conclusions. A broad variety of conditions can affect the pregnant patient, both during and immediately after pregnancy. Sonography can show many of these
disease processes, with computed tomography and magnetic resonance imaging useful selectively as
supplementary tools. Key words: complications of pregnancy; maternal; ultrasound.
Abbreviations
CT, computed tomography; HELLP, hemolysis, elevated
liver enzymes, and low platelets; IVC, inferior vena cava;
MRI, magnetic resonance imaging; RI, resistive index
Received July 22, 2002, from the Department of
Radiology, Harvard Medical School, Brigham and
Women’s Hospital, Boston, Massachusetts USA.
Revision requested July 31, 2002. Revised manuscript accepted for publication September 23,
2002.
I gratefully acknowledge the following colleagues
in the Department of Radiology at Brigham and
Women’s Hospital who contributed cases to this presentation: Carol B. Benson, MD, Douglas L. Brown,
MD, Mary C. Frates, MD, Faye C. Laing, MD, and Eric
van Sonnenberg, MD.
Address correspondence and reprint requests to
Donald Di Salvo, MD, Department of Radiology,
Brigham and Women’s Hospital, 75 Francis St,
Boston, MA 02115 USA.
W
hen examining the pregnant patient, the
sonographic imager really has 2 interrelated
but separate beings to consider. Although
much of obstetric sonography has been
focused on the fetus, sonography also plays a major role
in diagnosing illness in the mother. Some diseases are
common and can occur in both pregnant and nonpregnant patients; other conditions are unique to pregnancy.
This image presentation highlights several common and
less common maternal conditions and illustrates the role
of sonography in reaching the diagnosis. When the sonogram is inconclusive, the utility of magnetic resonance
imaging (MRI) and tailored computed tomography (CT)
will be shown.
Materials and Methods
Cases illustrating a range of pathologic conditions affecting women during and immediately after pregnancy
were collected from personal experience as well as
© 2003 by the American Institute of Ultrasound in Medicine • J Ultrasound Med 22:69–89, 2003 • 0278-4297/03/$3.50
Sonographic Imaging of Maternal Complications of Pregnancy
departmental teaching files. The primary imaging modality was sonography, with CT and MRI
used as needed. Cases were organized primarily
by anatomic region (i.e., liver and biliary tract,
kidney and ureters, bowel, ovary, and uterus and
placenta) as well as by onset (i.e., prepartum or
postpartum).
Case Descriptions
Prepartum Maternal Complications
Pregnancy and the Liver
Pregnancy-induced hypertension is a disease
process that can affect the maternal liver, kidneys,
and brain; it includes the clinical syndromes of
preeclampsia and eclampsia. The underlying
pathophysiologic characteristic of both of these
conditions is abnormal vasoconstriction coupled
with hyperreactive vascular smooth muscle.
Beginning in 1982, a variant of severe preeclampsia characterized by right upper quadrant
pain, nausea, vomiting, and abnormal liver
chemical levels and blood smear results was recognized. It was called the HELLP syndrome, an
acronym for hemolysis, elevated liver enzymes,
and low platelets.1 The pathophysiologic process
of this condition begins with arteriolar vasospasm, which causes endothelial damage and
fibrin deposition in the vessel lumen. This leads
to the following events: (1) platelet deposition on
the fibrin aggregates, reducing the number of circulating platelets; however, unlike disseminated
intravascular coagulation, coagulation factors
are not involved; (2) hematocyte destruction by
the fibrin aggregates (a microangiopathic
hemolytic anemia), leading to abnormal cells in
the peripheral smear (burr cells and schistocytes), an elevated indirect bilirubin level, and
anemia; and (3) hepatocyte destruction due to
hepatic microemboli (increased liver function
test levels) and distention of the liver due to
impeded blood flow (right upper quadrant
pain).2 In severe cases the parenchyma ruptures
and either forms a hepatic subcapsular hematoma or leads to exsanguination.
The prevalence of HELLP is 2% to 12% of
patients with preeclampsia or 1 per 150 live
births. Maternal risk factors include nulliparity,
young age (second and third decades), black
race, familial predisposition, and underlying diseases such as hypertension, diabetes, and renal
disease.3 Maternal mortality is 3.5%, usually
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because of liver rupture, which occurs when the
diagnosis is not suspected and treatment (emergent delivery) is delayed.1,3 The importance of
recognizing this uncommon syndrome is because (1) it can mimic other common disorders
(cholecystitis, biliary colic, and hepatitis), and (2)
it can occur without the classic triad of
preeclampsia. Sonography can play an important role in the diagnosis, both by excluding biliary tract disease and by identifying altered
hepatic and renal echo textures. Possible findings
include geographic, patchy areas of increased
echogenicity in the liver, diffusely increased renal
echo texture and size, perirenal fluid, and hepatic subcapsular hematoma (Figs. 1–3).4,5 Contrastenhanced abdominal CT and cranial MRI may
show characteristic changes in liver enhancement and brain signals, respectively.
Biliary tract disease is 4 times as common in
women as in men because of 2 effects of estrogen: decreased bile salt concentration and
increased cholesterol secretion into bile, both of
which contribute to cholesterol stone formation.
Additionally, an elevated progesterone level in
pregnancy, by relaxing the smooth muscle of the
gallbladder, decreases gallbladder contractility
and promotes bile stasis and stone formation.6
Sonographic findings with biliary disease include
gallstones, sludge, wall thickening, the sonographic Murphy sign, biliary dilatation, and ductal stones (Fig. 4).
Pregnancy and the Kidney
Hydronephrosis in pregnancy, also called
overdistension syndrome, occurs in more than
80% of pregnancies, begins as early as 11 to 15
weeks, and progresses through to term.7 Parity
and prior renal disease do not affect the degree of
dilatation. The cause of this syndrome is a combination of hormonal and mechanical factors.
Higher than usual levels of progesterone in pregnancy cause smooth muscle relaxation of the
ureters, increasing their capacitance. Mechanical
compression of the ureters between the pelvic
brim and the enlarged uterus also contributes to
ureteral dilatation and hydronephrosis. Rightsided predominance (3:1) is usually ascribed to
dextrorotation of the pregnant uterus and
increased distention of the right ovarian vein,
both of which can compress the right ureter.8
Rupture of a fornix and urinoma formation are
rare in the absence of ureteral calculi. A literature
review covering 50 years yielded 14 cases, 11 of
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Di Salvo
A
B
Figure 1. HELLP syndrome: patient with a twin gestation at 25 weeks with right upper quadrant pain and clinically suspected cholecystitis. Sagittal (A) and transverse (B) right upper quadrant sonograms show patchy echogenic areas in the liver. Note the geographic
shape and absence of vascular displacement. The gallbladder (not shown) was normal. Worsening hypertension and falling platelets
prompted emergency cesarean delivery, with subsequent resolution of all signs and symptoms.
which were right sided (Fig. 5). Four occurred in
the second trimester, with the remainder being
in the third trimester or at term.8 Symptomatic
patients can be successfully treated by sonographically guided retrograde stent placement
to relieve the obstructed system. Caution should
be taken when making the sonographic diagnosis of urinoma, because distention of renal
capsular vessels in pregnancy may simulate
perinephric fluid (Fig. 6).
Sonographic diagnosis of ureteral stones in
pregnancy presents a unique challenge because
of the underlying frequent asymmetric dilatation of the collecting systems described above.
Studies evaluating the intrarenal resistive index
(RI) in asymptomatic pregnant patients have
shown that both right and left kidneys have similar RIs, and there is no change in RIs during
pregnancy.9,10 In the absence of underlying renal
disease, however, a difference of greater than 0.1
in RIs should prompt further sonographic confirmation of mechanical ureteral obstruction.
This would include unilateral absence of a distal
ureteral jet or direct visualization of a stone
either at the ureterovesical or ureteropelvic junction (Fig. 7). Unilateral absence of a ureteral jet
with the patient supine should always be confirmed by reevaluation with the patient in the
contralateral decubitus position, because the
cause of the absent jet may merely be compression of the ureter by the uterus rather than an
obstructing calculus.11
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The transvaginal approach for the diagnosis of
distal ureteral calculi should be used whenever
the distal ureter is not adequately seen transabdominally and when there is a strong clinical
suggestion of obstruction.12 This is especially
true in the third trimester, when the fetal head
obscures the trigone (Figs. 8 and 9). Care must
be taken not to confuse a pelvic phlebolith with
a ureteral calculus. If a dilated ureter is not seen
proximal to the suspected “stone,” then the diagnosis of a phlebolith should be considered
Figure 2. HELLP syndrome with hepatic infarcts: patient with
lupus, tachycardia, and right upper quadrant pain at 27 weeks’
gestation. A pulmonary embolus was suspected clinically.
Contrast-enhanced CT shows geographic hypodense areas,
without a mass effect on hepatic vessels, compatible with
infarcts. The patient was treated with emergent delivery.
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Sonographic Imaging of Maternal Complications of Pregnancy
A
B
Figure 3. Postpartum HELLP syndrome with hepatic subcapsular hematoma: patient 8 days postpartum with fever, a decreasing hematocrit level, and right upper quadrant pain. A, Transverse right upper quadrant sonogram shows complex subcapsular fluid collection,
a small amount of free fluid, and gallbladder sludge. B, Contrast-enhanced CT shows subcapsular hematoma.
Figure 4. Acute cholecystitis and choledocholithiasis: 2 patients
with right upper quadrant pain and abnormal liver function test
results in the second trimester. A, Right upper quadrant sonogram shows sludge, stones, and wall thickening. B, Sagittal
sonogram through the distal common bile duct in another
patient shows a ductal stone with distal acoustic shadowing.
Figure 5. Urinoma complicating hydronephrosis of pregnancy:
patient with right flank pain at 27 weeks’ gestation. A, Sagittal
sonogram shows moderate to severe right hydronephrosis. The
patient was treated conservatively and had abatement of symptoms. B, Follow-up transverse image of the right kidney 1 week
after A reveals moderate perinephric urinoma and resolution of
hydronephrosis.
A
A
B
B
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Di Salvo
Figure 6. Distended renal capsular veins in pregnancy simulating
urinoma: patient with symptomatic physiologic hydronephrosis of
pregnancy. A and B, Sagittal (A) and transverse (B) right renal
sonograms show moderate hydronephrosis and a thin crescent of
fluid around the kidney, raising the suggestion of urinoma.
C, Color Doppler image shows flow from the suspected “urinoma.” Pulsed interrogation (not shown) confirmed a venous signal.
Figure 7. Distal right ureteral stone in pregnancy: patient at 14
weeks’ gestation with acute right flank pain and hematuria.
A, Sagittal right renal sonogram shows moderate hydronephrosis
and hydroureter. B, Borderline elevated RI of 0.68 in the right kidney. The RI of the left kidney (not shown) was 0.55. C, Oblique
transabdominal image through the urinary bladder shows an
obstructing distal right ureteral stone (between calipers).
A
A
B
B
C
C
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Sonographic Imaging of Maternal Complications of Pregnancy
Figure 8. Diagrams showing transvaginal probe placement for
imaging the distal ureter (reader’s left) and resulting screen
image from such a scan with the expected location of the distal
ureter (reader’s right). ANT indicates anterior; B, bladder; POST,
posterior; R, rectum; SP, symphysis pubis; and UT, uterus.
Reproduced by permission from Radiology.12
(Fig. 10). Finally, if ureteral obstruction due to
stone disease is suspected but cannot be localized with sonography, then limited CT should be
performed (Fig. 11).
As in nonpregnant patients with renal calculi,
the distribution of calcifications in the kidney
provides a helpful diagnostic clue to the underlying cause: the finding of medullary nephrocalcinosis should prompt a search for an
underlying parathyroid adenoma (Fig. 12).
Pyelonephritis, generally an ascending infection from the bladder, is primarily a clinical
diagnosis, with sonography used to exclude
complications such as an abscess or pyonephrosis when symptoms do not clear after appropriate therapy. Occasionally findings such as global
renal enlargement with overall hypoechogeni-
Figure 9. Distal right ureteral calculus in late pregnancy: acute right flank pain and hematuria in a patient at 36 weeks’ gestation.
Transabdominal images of both kidneys (not shown) showed moderate right hydronephrosis with an elevated RI. A, Coronal transvaginal image of the bladder trigone shows a stone at the right ureterovesical junction (straight arrow) with a proximal hydroureter (curved
arrow). The maternal bladder (b) is to reader’s left. The ureteral wall is thickened; note the dilated periureteral vessels. B, Same image
with color Doppler sonography shows hyperemia of the ureteral wall and dilated periureteral veins. This stone could not be seen transabdominally because of shadowing from the fetal head.
A
B
Figure 10. Pelvic phlebolith mimicking a distal ureteral stone: pregnant patient with hematuria, right flank pain, and right
hydronephrosis. A transvaginal scan was performed in an attempt to visualize the distal ureter. A, Coronal transvaginal image of the
right bladder trigone shows an echogenic shadowing focus indicative of a stone, but no proximal hydroureter could be seen. A phlebolith was suspected. B, Same image with color Doppler sonography shows dilated perivesical veins adjacent to calcification, confirming the impression of a phlebolith.
A
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B
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Di Salvo
city and perinephric fluid may be seen with
uncomplicated pyelonephritis; focal pyelonephritis may manifest as localized cortical
hyperechogenicity (Fig. 13). This should be followed to its resolution, because a renal abscess
may develop in an area of focal inflammation.
Pregnancy and the Bowel
With the notable exception of appendicitis,
sonography is not a first-line diagnostic tool for
bowel diseases. The familiar sonographic diagnostic criteria for appendicitis (a noncompressible, nonperistaltic, tender, tubular structure
with a diameter of >6 mm) apply in pregnant
patients, although the examination may be technically more difficult to perform because of
bowel displacement by the gravid uterus (Fig.
14). Left lateral decubitus positioning of the
patient may assist in bringing the cecum closer
to the anterior abdominal wall. Although other
types of bowel disease may be incidentally found
on sonography, limited CT is warranted whenever sonography is unsuccessful in showing the
appendix or other clinical diagnoses (e.g., diverticulitis, intussusception, and volvulus) are suspected (Fig. 15).
Figure 11. Obstructing proximal right ureteral stone with urinoma formation: fever, elevated white blood cell count, and right
flank pain in a patient at 28 weeks’ gestation. Appendicitis was suspected on clinical grounds. A, Sagittal right upper quadrant sonogram shows moderate hydronephrosis and perinephric fluid collection. The RIs were elevated, but no stone could be identified.
B, Non–contrast-enhanced axial CT shows an obstructing proximal ureteral stone, which was subsequently removed cystoscopically.
A
B
Figure 12. Medullary nephrocalcinosis secondary to parathyroid adenoma: pregnant patient with hematuria and flank pain in the
first trimester. A, Sagittal right renal sonogram shows hyperechoic medullary pyramids consistent with medullary nephrocalcinosis. The
left kidney showed similar findings. The patient was subsequently found to be hypercalcemic. B, Transverse image through the left
side of the neck shows a large hypoechoic mass posterior to the left thyroid lobe consistent with a large parathyroid adenoma. This
was confirmed surgically after delivery.
A
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B
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Sonographic Imaging of Maternal Complications of Pregnancy
A
B
Figure 13. Focal right pyelonephritis: patient at 32 weeks’ gestation with right flank pain and an elevated white blood cell count.
Sagittal (A) and transverse (B) right renal sonograms show focal wedge-shaped cortical hyperechogenicity in the upper pole. This
resolved after antibiotic therapy.
Pregnancy and the Ovary
Ovarian masses encountered in pregnancy
include hormonally responsive cysts (corpus
luteum of pregnancy and theca lutein cysts) and
other cysts or masses that may be incidentally
detected during an obstetric sonogram (cystadenoma, dermoid, pedunculated fibroid, and ovarian cancer). The sonographic appearance of
many of these masses has been well described
Figure 14. Appendicitis: fever and right lower quadrant pain in patient at 20
weeks’ gestation. Transverse split screen image of the right lower quadrant shows
a thickened appendix with a small amount of free fluid. Scans without (left) and
with (right) compression show no change in the appearance of the abnormally
dilated appendix.
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and is often specific enough to offer a reasonable
differential diagnosis (Fig. 16).13 The decision for
surgical intervention depends on the sonographic findings (thickened irregular septations,
mural nodules, indeterminate solid elements,
and ascites), the likelihood of torsion or dystocia,
and the stage of pregnancy. In the first trimester,
risk of spontaneous abortion is highest, and in
the third trimester, risk of preterm labor is highest, so the second trimester is generally the time
for exploration of persistent and worrisome
adnexal masses.6
The corpus luteum of pregnancy is sustained by
the luteinizing hormone–like effect of β-human
chorionic gonadotropin (β-hCG) and in turn is a
source of progesterone, which maintains the uterine decidua for the developing gestation (Fig. 17).
It typically involutes by the end of the first
trimester, as the hCG levels fall and the placenta
becomes the primary source of progesterone,
although it may persist through weeks 16 and 17.6
Although usually anechoic, the corpus luteum
may have internal echoes or septa due to hemorrhage (Fig. 18). Unfortunately, color Doppler
sonography is not helpful for distinguishing these
complex cysts from malignancy, because both
typically display a low-resistance waveform (Fig.
17B). Rare complications of corpus luteal cysts
include rupture and torsion (see below).
Theca lutein cysts (hyperreactio luteinalis) represent excessive luteal cyst formation due to
unusually high levels of hCG. Although most
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Di Salvo
A
B
Figure 15. Pseudomembranous colitis: patient at 24 weeks’ gestation with diarrhea, fever, and right lower quadrant pain. The
patient was undergoing concurrent antibiotic therapy for periorbital cellulitis. A, Transverse sonogram through the right lower quadrant shows an abnormally echogenic and thickened (18-mm) cecal wall. A fluid-filled structure thought to be the appendix is shown
inferiorly. B, Sagittal sonogram through the right flank (the right kidney is shown at the top edge) shows thickening of the cecum.
Subsequent abdominal CT showed pancolitis and a normal appendix. Stool cultures were positive for Clostridium difficile.
often seen with gestational trophoblastic disease,
they can rarely occur with multiple gestations or
with fetal hydrops (perhaps reflecting the
increased placental mass in these instances).14 A
benign solid ovarian mass that is occasionally
seen is the pregnancy luteoma, which represents
ovarian stromal hyperplasia (Fig. 19). Unlike
hyperreactio luteinalis, this lesion is not associated with elevated levels of hCG. Because of
stromal androgen production, there is a 25%
incidence of maternal virilization.15
Ovarian torsion during pregnancy is facilitated
by the presence of the corpus luteum in the first
trimester, although any preexisting mass or large
cyst following ovulation induction may be an
inciting factor (Fig. 20). Sonographic diagnosis
relies on gray scale findings of unilateral ovarian
enlargement, an unusual position of the symptomatic ovary, and the presence of free fluid. The
role of Doppler sonography in excluding the
diagnosis is limited, because torsion may be
intermittent, so the presence of flow may be
falsely reassuring. However, the unilateral
absence of flow or marked reduction of flow on
the symptomatic side (assuming technical
parameters are correctly set) provides confirmation of the diagnosis in the proper clinical setting
(Fig. 21).
tractions can simulate fibroids, but helpful distinguishing features include (1) shape analysis:
contractions typically bulge into the uterine cavity, whereas fibroids exert a mass effect equally
in all directions; (2) echo texture: contractions
are either hypoechoic or isoechoic, whereas
fibroids are hypoechoic and sound attenuating,
with edge shadowing artifacts; and (3) time: contractions typically change shape, location, or
both within 30 to 40 minutes (Fig. 23).
Figure 16. Mucinous cystadenoma: 33-year-old patient at 36
weeks’ gestation with poor prenatal care; a 12-cm left ovarian
complex cyst was incidentally found. Transverse image of left
adnexa shows a multilocular cyst (between calipers) with irregular wall and internal low-level echoes located just to the left of
the gravid uterus. The mass was removed during elective cesarean delivery 3 weeks later.
Pregnancy and the Uterus
Uterine fibroids are the most common solid
masses in pregnancy, with prevalence ranging
from 0.3% to 2.6% (Fig. 22). Braxton Hicks conJ Ultrasound Med 22:69–89, 2003
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Sonographic Imaging of Maternal Complications of Pregnancy
A
B
Figure 17. Normal corpus luteum of pregnancy: patient at 6 weeks’ gestation with bleeding. A, Transverse transabdominal sonogram shows a thick-walled left ovarian cyst, typical of the corpus luteum. B, Transvaginal color Doppler image of the left corpus luteum
shows typical peripheral vascularity with a low RI (0.43).
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The growth of fibroids in pregnancy is governed by competing hormonal and vascular
factors. Estrogen receptors are thought to be at
higher concentrations on myoma cells than in
normal myometrium, so the elevated estrogen
level in early pregnancy promotes growth.
Progesterone, typically elevated later in pregnancy, is thought to inhibit fibroid growth.
Additionally, uterine stretching may interfere
with arterial supply to fibroids, promoting
infarction and cystic degeneration in later pregnancy. Patients with these complications can
have acute pelvic pain (Figs. 24 and 25). A study
that followed myoma volume prospectively
through pregnancy and into the puerperium
found only 32% of cases with enlargement
(defined as a >10% volume change), and all
appreciable growth was confined to the first
trimester. Considerable involution of fibroids
occurred in the 4 weeks after delivery. Growth
was independent of myoma volume, but complications (increased preterm delivery and
cesarean delivery rate and intrauterine growth
restriction) were noted in the largest myomas
(>200 cm3).16
Figure 18. Hemorrhagic corpus luteum of pregnancy: patient at
5 weeks’ gestation with acute right lower quadrant pain.
Transverse sonogram shows solid right adnexal mass, raising
concern for ectopic pregnancy. A follow-up scan confirmed
intrauterine pregnancy and showed gradual resolution of the
hemorrhagic right corpus luteum.
Figure 19. Pregnancy luteoma: incidental discovery on a thirdtrimester sonogram done to check fetal growth. Transverse
sonogram of right adnexa at 30 weeks’ gestation shows a 10cm solid mass. Images of the right ovary in the first trimester
(not shown) were normal.
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Adenomyosis, an elusive diagnosis in nonpregnant women, is even more difficult to
detect during pregnancy, given the ease with
which it can be confused with contractions or
fibroids on sonography (Fig. 26). However, persistent nonfocal myometrial thickening should
raise the suggestion of this entity. Color Doppler
sonography may be useful for confirming the
nonfocal nature of the area in question, as
opposed to the peripheral feeding vessels typically seen with uterine fibroids.17
Figure 21. Ovarian torsion in the second trimester: patient with
episodic right lower quadrant pain at 26 weeks’ gestation.
A, Transverse sonogram of right adnexa shows a 5-cm solid right
mass thought to be an enlarged ovary. A small amount of free
fluid (not shown) was also seen. B, Transverse color Doppler
image of the left ovary shows a normal intraovarian lowresistance arterial signal. C, Transverse Doppler image through the
enlarged right ovary shows faint mixed arterial and venous signals. Exploratory laparotomy revealed an edematous ovary with
270° torsion, which was repaired. A follow-up sonogram 1 week
after surgery showed a decrease in ovarian size with preserved
blood flow. The pregnancy continued uneventfully to term.
A
Figure 20. Torsion of the corpus luteum: patient at 6 weeks’
gestation with acute pelvic pain. A, Sagittal midline sonogram
shows a 6-mm living intrauterine pregnancy (between calipers).
A large cyst is shown interposed between the uterus and bladder (B). B, Transverse sonogram shows that the cyst is a corpus
luteum that is part of an enlarged, torsed left ovary (between
calipers). Free fluid (not shown) was also present. The patient
underwent emergency detorsion but had a spontaneous abortion 3 days after surgery.
B
A
B
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c
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Sonographic Imaging of Maternal Complications of Pregnancy
Figure 22. Uterine fibroid in pregnancy: asymptomatic patient
at 20 weeks’ gestation examined for fetal growth. Transverse
sonogram through the right fundus shows a small subserosal
fibroid (between calipers). Note the typical hypoechoic appearance, refractive shadows, and mass effect equally exerted in all
directions.
Uterine rupture has an incidence of 0.73 per
10,000 deliveries, with most cases occurring in
the third trimester at the site of a cesarean delivery scar.18,19 Other risk factors include uterine
anomalies (unicornuate uterus), prior uterine
curettage, persistent retroflexion due to adhesions (“trapped uterus”), prior uterine surgery,
and cornual implantation (Fig. 27). Classic
symptoms include pain, vaginal bleeding, and
hypotension, but with dehiscence of a scar
(defined as myometrial separation only), the
symptoms are less dramatic. Fifty percent of
ruptures from dehiscent scars are not diagnosed until delivery, resulting in a fetal mortality rate of 22%. Delayed diagnosis until the
postpartum period may lead to a bladder flap
hematoma (see below and Fig. 33).20 Sonographic findings during pregnancy include
extrauterine hematoma, fetal parts, or both
(especially during the first trimester), intraamniotic hemorrhage, and focal bulging of
membranes through the site of dehiscence.
Abnormal placental attachment to the uterine wall (placenta accreta, increta, and percreta) is a major maternal risk. Placenta accreta is
defined pathologically by villi in direct contact
with myometrium without intervening endometrial decidua. With placenta increta, penetration is deeper, into the myometrium,
whereas placenta percreta has villi extending
to the uterine serosa, sometimes with invasion
of adjacent tissue (bowel and bladder). Lifethreatening hemorrhage can occur at delivery
due to failure of placental separation from the
uterine wall and can necessitate hysterectomy.
Major risk factors include prior uterine instrumentation or surgery (especially prior cesarean delivery) and placenta previa, because
uterine decidua is deficient at sites of scarring
and in the lower uterine segment. The risk of
both placenta previa and accreta increases
dramatically with prior cesarean deliveries: if
previa is present, the risk of accreta is 5% with
no prior cesarean deliveries, 24% with 1 prior
Figure 23. Braxton Hicks contraction: asymptomatic patient at 22 weeks’ gestation examined for fetal growth. A, Sagittal sonogram shows retroplacental contraction, which typically bulges in only the inner myometrial contour. Although the contraction is
hypoechoic, no refractory shadows are shown. B, Sagittal sonogram through the same area 10 minutes later shows partial resolution of the contraction.
A
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B
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A
B
Figure 24. Cystic degeneration of pedunculated fibroid: patient examined initially for size greater than dates at 12 weeks' gestation, with follow-up done at 20 weeks' gestation for acute right lower quadrant pain. A, Transverse image at 12 weeks
through the right side of the uterus shows a solid pedunculated fibroid. B, Follow-up at 20 weeks through the same area shows
central cystic degeneration of the fibroid, which mimics an ovarian cyst.
cesarean delivery, and 48% with 2 or more
cesarean deliveries.21 Sonographic features
are loss of the normal hypoechoic myometrial
layer beneath the placenta, large placental
vascular spaces, loss of the hyperechoic uterine serosa–bladder interface, and extrauterine
or intravesical masses (Figs. 28 and 29).22
Given that cesarean delivery rates are as high
as 17% to 20% in the United States, screening
of such patients in subsequent pregnancies is
advisable.
Postpartum Maternal Complications
Postpartum complications include extraperitoneal hematomas (subfascial, bladder flap,
and broad ligament), local uterine complications (retained products of conception and
hematometra), and ovarian vein thrombophlebitis.
Subfascial hematoma occurs behind the rectus
muscles in the prevesical space and the inferiorly contiguous retropubic space of Retzius, due to
disruption of inferior epigastric vessels during
Figure 25. Hemorrhagic degeneration of fibroid: patient seen at 29 weeks’ gestation for left-sided pain and a palpable mass.
A, Transverse sonogram shows a 12-cm complex left-sided mass (between × calipers) with an intrauterine fetus (between + calipers)
toward the maternal right side. Because of the large size of the mass, its origin (uterine versus ovarian) was uncertain, and further
examination with pelvic MRI was done. B, T2-weighted axial MR image shows the high-signal mass arising from the left side of the
uterus. The mass also had a high signal on T1-weighted imaging and was not suppressed with fat saturation. This was consistent
with hemorrhagic degeneration, which was confirmed at subsequent cesarean delivery.
A
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A
B
Figure 26. Adenomyosis: patient seen initially at 8 weeks’ gestation for sizing and subsequently at 32 weeks for preterm labor.
A, Sagittal sonogram at 8 weeks shows diffuse posterior myometrial thickening thought to represent a contraction. B, Transverse
sonogram at 32 weeks shows retroplacental thickening thought to represent a fibroid. The patient gave birth 2 weeks later.
Hysterectomy 1 year later for pelvic pain showed diffuse adenomyosis and no fibroids.
surgery (Fig. 30). This is a large potential space
(accommodating up to 3 L), which can dissect
superficially between the rectus muscles to
appear as a subcutaneous collection; it may also
dissect through the umbilicovesical fascia to the
extraperitoneal space around the uterus (bladder
flap and broad ligament).23 Sonography over the
anterior abdominal wall reveals a complex fluid
collection anterior and superior to the bladder,
crossing the midline (Fig. 31).
Bladder flap hematoma occurs adjacent to the
incision in the lower uterine segment beneath
the peritoneal fold that was incised, reflected,
and then reapproximated during cesarean delivery (Fig. 32).24 It may extend laterally along the
broad ligaments into the retroperitoneum. The
source of bleeding is usually injury of uterine
vessels during surgery, although an occult dehiscence may be the underlying cause (Fig. 33). The
clinical symptoms are similar to those seen in
subfascial hematomas, but an adnexal mass or
flank pain due to renal obstruction may be the
initial symptom for a broad-ligament hematoma (Fig. 34). Typical sonographic findings
Figure 27. Trapped uterus at 13 weeks: patient with a history of pelvic inflammatory disease undergoing obstetric sonography for
size less than dates. A, Sagittal sonogram shows an apparent vertex fetus, who appears unusually deep within the maternal pelvis.
The cervix is not shown. B, Sagittal image shows the cervix and sharply retroflexed fundus with a posterior placenta closely apposed
to the maternal spine. Spontaneous abortion occurred 2 weeks later.
A
82
B
J Ultrasound Med 22:69–89, 2003
Di Salvo
A
Figure 28. Placenta percreta at 28 weeks: patient with severe
right lower quadrant pain who had a history of surgical repair
of a right unicornuate uterus. Transverse sonogram through the
right fundus shows the absence of a normal subplacental
myometrium. Gravid hysterectomy showed a focal percreta at
the prior surgical scar.
include a heterogeneous solid mass between
the lower uterine segment and the posterior
bladder wall (Fig. 35). This may extend superiorly to indent the dome of the bladder. As distinguished from the normal slight irregularity of
the lower uterine segment after cesarean delivery, the bladder flap hematoma has been
described as a mass at least 2 cm in mean diameter.25 Over several weeks it evolves to a cystic
collection (seroma).
Retained products of conception are uncommon complications of pregnancy. They can lead
to prolonged postpartum hemorrhage and
endometritis. Curettage is the standard treatment, although not without notable complications (7%) of uterine perforation, cervical
laceration, and (delayed) synechia formation.
Unfortunately, sonographic findings are often
nonspecific, because blood clots and retained
products show considerable overlap in sonographic appearance. Sonography can be most
helpful in excluding the diagnosis if a thin (2mm) endometrial stripe or simple endometrial
fluid is seen. Solid echogenic masses in the
lumen or uterine wall are the most specific findings for a retained placenta (Fig. 36).26 I have
also noted anecdotally that low-resistance
Doppler signals in these masses can also be
predictive (Fig. 37). However, when using
Doppler sonography in this setting, it is important not to confuse low-resistance arterial signals that arise within the myometrium (which
J Ultrasound Med 22:69–89, 2003
B
C
Figure 29. Placenta percreta and hemoperitoneum: patient
with abdominal pain at 15 weeks’ gestation. A, Sagittal midline
sonogram shows a vertex fetus, the cervix, and complex cul-desac fluid. The initial impression was a ruptured cyst, and the
patient was treated conservatively. B, Follow-up right upper
quadrant sonogram 1 week later (when the patient returned
with increasing pain and hypotension) shows moderate
hemoperitoneum surrounding the liver. C, Sagittal image
through the uterine fundus shows an anterior placenta, which
focally invades the uterine wall (arrow). Emergency gravid hysterectomy confirmed placenta percreta.
83
Sonographic Imaging of Maternal Complications of Pregnancy
Figure 30. Schematic sagittal view of the female pelvis showing
extraperitoneal spaces. Subfascial hematomas occupy the prevesical space and may extend inferiorly to the space of Retzius.
bl indicates urinary bladder; per, peritoneum; pre, prevesical
space; ra, rectus abdominis muscle; rp, retropubic space (of
Retzius); tf, transversalis fascia; ut, uterus; and uvf, umbilicovesical fascia. Reprinted by permission from AJR.23
Figure 31. Subfascial hematoma in a patient with a falling
hematocrit level after cesarean delivery. Sagittal midline sonogram shows large complex fluid collection (between calipers)
beneath the anterior abdominal wall indenting the dome of the
bladder.
84
represent the placental implantation site) with
similarly appearing Doppler signals arising from
tissue within the endometrial cavity (which represent retained products). Occasionally, there
can be delay in involution of the placental
implantation site vessels that can be the cause of
postpartum bleeding, called subinvolution of
the placental vascular bed (Fig. 38).27
Postpartum ovarian vein thrombophlebitis is
an uncommon (0.15%–0.18% prevalence) disorder involving thrombosis and inflammation of
one or both ovarian veins.28,29 The right side is
affected 5 times as often as the left. Predisposing
factors include venostasis, cesarean delivery,
and endometritis.19 Sonographic findings
include ovarian enlargement and thrombosis of
the adjacent ovarian vein (Figs. 39 and 40).
Although the pelvic portion of the right ovarian
vein is usually obscured by bowel gas, the
abdominal portion (the junction of the vein with
the inferior vena cava [IVC] near the renal hilus)
is more amenable to sonographic visualization
with the patient in the right anterior oblique
position. Doppler sonography should be used to
confirm presence or absence of flow, because a
dilated but patent ovarian vein is often seen in
the puerperium (Fig. 41).
Figure 32. Diagram of the typical location of a bladder flap
hematoma. Although it is usually in the potential space between
the lower uterine segment and bladder (shown in black), it may
extend superiorly to the extraperitoneal spaces superior to the
bladder and uterus (shown by diagonal lines). The peritoneum is
represented by the heavy black line. Reproduced by permission
from the Journal of Ultrasound in Medicine.24
J Ultrasound Med 22:69–89, 2003
Di Salvo
A
B
Figure 33. Infected bladder flap hematoma and uterine dehiscence: patient with fever after cesarean delivery. A, Pelvic CT after
administration of an intravenous contrast agent shows a stellate hypodense area extending through the uterine wall, extending from
the uterine cavity into small periuterine fluid collection. B, Fistulogram obtained after percutaneous drainage of an infected periuterine collection shows the injected contrast medium outlining the area of dehiscence. The patient was treated conservatively with
antibiotics and had spontaneous closure of the fistula.
A
B
Figure 34. Broad ligament hematoma causing hydronephrosis: patient with a falling hematocrit level after cesarean delivery.
A, Transverse sonogram shows complex fluid collection in the left adnexa immediately beneath the broad ligament (arrows). The
uterus is displaced toward the patient’s right side. B, Sagittal image of the left kidney and proximal ureter shows moderate
hydronephrosis. Both the hematoma and the hydronephrosis were treated conservatively and resolved gradually over 1 month.
Figure 35. Bladder flap hematoma in a patient examined for
bleeding after cesarean delivery. Sagittal midline sonogram
shows a small isoechoic mass (between calipers) anterior to the
lower uterine segment
J Ultrasound Med 22:69–89, 2003
Figure 36. Retained placenta in a subseptate uterus: patient
with continuous postpartum bleeding. Transverse image through
the uterine fundus shows a large echogenic mass expanding on
the left side; the normal right fundus is empty. This patient was
treated by sonographically guided dilation and curettage.
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Sonographic Imaging of Maternal Complications of Pregnancy
A
B
Figure 37. Retained products of conception: patient with continuing bleeding after spontaneous abortion in the first trimester.
A, Sagittal midline sonogram shows solid material (between calipers) in the uterine cavity. The differential diagnosis included
hematometra and retained products. B, Sagittal color Doppler image through the same area shows flow within the solid material,
indicating retained products, which was confirmed by dilation and curettage.
A
B
Figure 38. Placental implantation site: patient with prolonged bleeding 1 week after vaginal delivery. A, Transverse color Doppler
sonogram through the uterine fundus shows a small amount of fluid in the endometrial cavity. A prominent vessel is shown in the
right posterior myometrium. B, Transverse image with pulsed Doppler interrogation of the vessel previously identified shows a lowresistance arterial signal representing subinvolution of the placental vascular bed. This patient was treated with ergot, and the bleeding abated.
A
B
Figure 39. Postpartum ovarian vein thrombophlebitis: 2 patients with fever and right lower quadrant pain after cesarean delivery.
A, Sagittal sonogram through right adnexa shows an enlarged right ovary, a tubular structure (between calipers) posteriorly, and free
fluid inferiorly. This ovarian vein thrombosis did not extend proximally. B, Transverse image through the upper abdomen and liver in
a different patient shows a dilated right ovarian vein (arrow) anterolateral to the IVC and aorta.
86
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Di Salvo
A
B
C
D
Figure 40. Retained products and septic ovarian vein thrombophlebitis: patient with postpartum fever and vaginal discharge.
A, Coronal sonogram of the right flank shows a tubular structure: a punctate echogenic focus with a ring-down artifact consistent
with air. B–D, Sequence of CT images shows a dilated, clot-filled right ovarian vein extending from the renal hilus into the pelvis. The
occluded vein compresses the IVC in B, and a focus of air is shown within the middle portion in C. The uterus in D is distended with
retained products.
Figure 41. Distended right ovarian vein: postpartum patient examined for fever. A, Coronal sonogram obtained through the right
flank shows a dilated right ovarian vein joining IVC. Thrombosis was initially suspected on the basis of the gray scale appearance.
B, Pulsed Doppler image obtained through the dilated vein shows venous signals indicating patency.
A
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B
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Sonographic Imaging of Maternal Complications of Pregnancy
Conclusions
Sonography is the imaging modality of choice for
diagnosing maternal disease both during and
after pregnancy. It is important for sonographic
imagers to be aware of the broad spectrum of
pathologic conditions that the pregnant patient
can have, many of which are unique or more
common in pregnancy. Familiarity with the
sonographic appearance of these conditions is
crucial, because patients will generally undergo
sonographic imaging first when problems arise.
Cognizance of sonography’s limitations is also
important, especially for the evaluation of bowelrelated problems and large atypical adnexal
masses or when the disease process targets multiple organ systems (i.e., HELLP syndrome); in
such instances, CT or MRI may be indicated.
References
1.
2.
Sibai BM, Taslimi MM, El-Nazer A, et al. Maternalperinatal outcome associated with the syndrome of
hemolysis, elevated liver enzymes and low platelets in
severe preeclampsia-eclampsia. Am J Obstet Gynecol
1986; 155:501–509.
3.
Knox TA, Olans LB. Liver disease in pregnancy. N Engl
J Med 1996; 335:569–576.
4.
Benacerraf BR, Frigoletto FD Jr, Martini CA. Sonographic findings in severe pre-eclampsia twenty-four
hours prior to clinical signs. Am J Obstet Gynecol
1985; 152:684–685.
5.
6.
7.
8.
88
Weinstein L. Syndrome of hemolysis, elevated liver
enzymes and low platelet count: a consequence of
hypertension in pregnancy. Am J Obstet Gynecol
1982; 142:159–167.
Kronthol AJ, Fishman EK, Kuhlman JE, Bohlman ME.
Hepatic infarction in preeclampsia. Radiology 1990;
177:726–728.
Fleischer AC, Shah DM, Entman SE. Sonographic
evaluation of maternal disorders during pregnancy.
Radiol Clin North Am 1990; 28:51–58.
Boridy IC, Maklad N, Sandler CM. Suspected urolithiasis in pregnant women: imaging algorithm and literature review. AJR Am J Roentgenol 1996; 167:
869–875.
Meyers SJ, Lee RV, Munschauer RW. Dilatation and
nontraumatic rupture of the urinary tract during
pregnancy: a review. Obstet Gynecol 1985; 66:809–
815.
9.
Nazarian GK, Platt JF, Rubin JM, Ellis JH. Renal duplex
Doppler sonography in asymptomatic women during
pregnancy. J Ultrasound Med 1993; 12:441–444.
10. Brkljacic B, Drinkovic I, Sabljar-Matovinovic M, et al.
Intrarenal duplex Doppler sonographic evaluation of
unilateral native kidney obstruction. J Ultrasound
Med 1994; 13:197–204.
11. Wachsberg RH. Unilateral absence of ureteral jets in
the third trimester of pregnancy: pitfall in color
Doppler US diagnosis of urinary obstruction.
Radiology 1998; 209:279–281.
12. Laing FC, Benson CB, Di Salvo DN, Brown DL, Frates
MC, Loughlin KR. Distal ureteral calculi: detection
with vaginal US. Radiology 1994; 192:545–548.
13. Bromley B, Benacerraf B. Adnexal masses during
pregnancy: accuracy of sonographic diagnosis and
outcome. J Ultrasound Med 1997; 16:447–452.
14. Fleming P, McLeary RD. Nonimmunologic fetal
hydrops with theca lutein cysts. Radiology 1981;
141:169–170.
15. Clement PB. Non-neoplastic disease of the ovary. In:
Kurman RJ (ed). Blaustein’s Pathology of the Female
Genital Tract. 3rd ed. New York, NY: Springer-Verlag;
1977:495–497.
16. Rosati P, Exacoustos C, Mancuso S. Longitudinal evaluation of uterine myoma growth during pregnancy.
J Ultrasound Med 1992; 11:511–515.
17. Hirai M, Shibata K, Sagai H, Sekiya S, Goldberg BB.
Transvaginal pulsed and color Doppler sonography
for the evaluation of adenomyosis. J Ultrasound Med
1995; 14:529–532.
18. Gale JT, Mahoney BS, Bowie JD. Sonographic features of rupture of the pregnant uterus. J Ultrasound
Med 1986; 5:713–714.
19. Rooholamini SA, Au AH, Hansen GC, et al. Imaging
of pregnancy-related complications. Radiographics
1993; 13:753–770.
20. Shrout AB, Kopelman JN. Ultrasonographic diagnosis of uterine dehiscence during pregnancy. J Ultrasound Med 1995;14:399–402.
21. Finberg HJ, Williams JW. Placenta accreta: prospective sonographic diagnosis in patients with placenta
previa and prior cesarean sections. J Ultrasound Med
1992; 11:333–343.
22. Hoffman-Tretin JC, Koengsberg M, Rabin A,
Anyaegbunam A. Placenta accreta: additional sonographic observations. J Ultrasound Med 1992; 11: 29–34.
J Ultrasound Med 22:69–89, 2003
Di Salvo
23. Wiener MD, Bowie JD, Baker ME, Kay HH. Sonography of subfascial hematoma after cesarean delivery. AJR Am J Roentgenol 1987; 148:907–910.
24. Winsett MZ, Fagan CJ, Bedi DG. Sonographic
demonstration of bladder-flap hematoma. J Ultrasound Med 1986; 5:483–487.
25. Baker ME, Bowie JD, Killam AP. Sonography of postcesarean-section bladder-flap hematoma. AJR Am
J Roentgenol 1985; 144:757–759.
26. Hertzberg BS, Bowie JD. Ultrasound of the postpartum uterus: prediction of retained placental tissue.
J Ultrasound Med 1991; 10:451–456.
27. Khong TY, Khong TK. Delayed postpartum hemorrhage: a morphologic study of causes and their relation to other pregnancy disorders. Obstet Gynecol
1993; 82:17–22.
28. Banan GN, Frisch KM. Duplex Doppler evaluation
of puerperal ovarian vein thrombosis. AJR Am
J Roentgenol 1987; 149:321–322.
29. Savader SJ, Otero RR, Savader BL. Puerperal ovarian
vein thrombosis: evaluation with CT, US and MR
imaging. Radiology 1988; 167:637–639.
J Ultrasound Med 22:69–89, 2003
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