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AJR 2001; 176:607-615
© American Roentgen Ray Society


Pictorial Essay

Hemorrhage During Pregnancy

Sonography and MR Imaging

Isabelle Trop1 and Deborah Levine

1 Both authors: Radiology Department, Beth Israel Deaconess Medical Center, 330 Brookline Ave., Boston, MA 02215.

Received April 3, 2000; accepted after revision August 4, 2000.

 
Presented at the annual meeting of the American Roentgen Ray Society, Washington, DC, May 2000.

Address correspondence to D. Levine.


Introduction
Top
Introduction
Hemorrhage Related to the...
Intraamniotic Bleeding
Umbilical Cord Hematoma
Bleeding Within the Fetus
Intracerebral Bleeding
Fetal Abdominopelvic Hemorrhage
Conclusion
References
 
Vaginal bleeding is the most frequent indication for first-trimester sonography. In the presence of a live embryo, the most frequently encountered sonographic finding is a subchorionic hematoma. Bleeding in the second and third trimesters is less common. Bleeding restricted by the placenta, the amniotic or chorionic membranes, or both has characteristic sonographic features that are important to recognize because the prognosis varies with location. Bleeding within the fetus is uncommon. This pictorial essay presents the varied sonographic and MR imaging manifestations of bleeding throughout pregnancy.


Hemorrhage Related to the Placenta and Intrauterine Membranes
Top
Introduction
Hemorrhage Related to the...
Intraamniotic Bleeding
Umbilical Cord Hematoma
Bleeding Within the Fetus
Intracerebral Bleeding
Fetal Abdominopelvic Hemorrhage
Conclusion
References
 
Separation of the placenta from the myometrium where it is implanted causes bleeding. When only the margin of the placenta is separated, it is called a marginal subchorionic hematoma (Fig. 1A,1B,1C). When the bleeding is behind the placenta, it is termed a retroplacental bleed. The term "abruption" (abruptio placentae) is typically reserved for premature placental separation occurring after 20 weeks. Subamniotic bleeding is a collection anterior to the placenta and limited by the umbilical cord (Fig. 1A,1B,1C).



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Fig. 1A. Drawings show classification of hematomas in and around placenta. P = placenta, red = hematoma, blue line = amnion, pink line = chorion. Retroplacental bleeding is found behind placenta.

 


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Fig. 1B. Drawings show classification of hematomas in and around placenta. P = placenta, red = hematoma, blue line = amnion, pink line = chorion. Subchorionic bleeding dissects chorion and endometrium; when such bleeding involves margin of placenta, it is called marginal subchorionic hematoma.

 


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Fig. 1C. Drawings show classification of hematomas in and around placenta. P = placenta, red = hematoma, blue line = amnion, pink line = chorion. Subamniotic hemorrhage is contained within amnion and chorion and thus extends anteriorly to placenta but is limited by reflection of amnion on placental insertion site of umbilical cord. Subamniotic bleeding is rare.

 

In early pregnancy, a hypoechoic collection is often seen adjacent to the gestational sac (Fig. 2A); when small, this collection is physiologic. Subchorionic hematomas manifest as crescentic collections lifting the chorionic membrane (Figs. 2B, 3A,3B, and 4). Depending on the time elapsed since the bleeding, the collection will have variable echotexture; it will be hyperechoic initially, with decreasing echotexture over time [1]. Most hematomas gradually decrease in size on follow-up [2]. A marginal subchorionic hematoma can mimic a twin gestational sac (Fig. 2B). Subchorionic bleeding dissecting around the endometrial cavity (Fig. 4) should be distinguished from chorioamniotic separation. Occasionally, prominent basal veins may mimic subacute hemorrhage (Fig. 5).



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Fig. 2A. Subchorionic bleeding in fetus at 5.5 weeks' gestational age. Transverse transvaginal sonogram reveals intrauterine gestational sac with yolk sac. Note small amount of blood (arrow) adjacent to gestational sac.

 


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Fig. 2B. Subchorionic bleeding in fetus at 5.5 weeks' gestational age. Transvaginal sagittal sonogram obtained 2 weeks after A because of vaginal bleeding shows subchorionic hematoma (arrow) with debris. Collection could be mistaken for second gestational sac with embryonic demise.

 


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Fig. 3A. Marginal subchorionic hematoma in 30-year-old woman with spotting at 15 weeks' gestational age. Transabdominal transverse sonogram of uterus shows heterogeneous collection of blood (arrow) lifting margin of placenta (arrowheads).

 


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Fig. 3B. Marginal subchorionic hematoma in 30-year-old woman with spotting at 15 weeks' gestational age. Transabdominal transverse sonogram shows hematoma in potential space between chorion (short solid arrow) and endometrium (long arrow). Note specular reflector of thin amnion (open arrow).

 


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Fig. 4. Distinction between subchorionic hematoma and unfused amnion in patient with vaginal bleeding at 13 weeks' gestational age. Transabdominal sagittal sonogram of uterus reveals subchorionic hematoma (H) extending posteriorly around chorion (arrows) and lifting edge of anterior placenta (P). Appearance should not be confused with that of unfused amnion. Amnion is thin membrane continuous along anterior placental edge but limited by umbilical cord insertion; subchorionic bleeding leads to edge of placenta.

 


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Fig. 5. Retroplacental veins mimicking hematoma at 36 weeks' gestational age. Transverse sonogram of placenta reveals hypoechoic structures (arrows) behind and at edge of placenta. Slow-moving particles were seen on real-time imaging. This appearance may mimic hematoma but is caused by retroplacental veins.

 

Correlation between the size of the subchorionic hematoma and the rate of pregnancy loss is imperfect. In general, small- and moderate-sized subchorionic hematomas have a better outcome than large ones [3]. The percentage of placental detachment is the prognostic factor most strongly associated with fetal mortality: the frequency of fetal demise is 50% for retroplacental hematoma versus 7% for marginal subchorionic hematoma [4].

Abruptio placentae is one of the most serious complications of pregnancy, accounting for up to 25% of perinatal deaths [1]. Diagnosis requires a high index of suspicion because the signs and symptoms are variable, including a painful tense uterus, vaginal bleeding, premature labor, fetal distress, and coagulopathy; most episodes remain asymptomatic. Sonographic findings are negative in most cases, either because of the passage of blood without accumulation behind the placenta or because of blood being isoechoic with the placenta. The only evidence of abruption may be the identification of an abnormally thick placenta [1]. The sensitivity of sonography is low, 2-20% [2]. The clinical visualization of a hematoma is important because pregnancies with demonstrable hematoma have a worse prognosis than when no hematoma can be seen [1]. MR imaging may differentiate hematomas of various ages from the placenta (Fig. 6A,6B). T1-weighted gradient-echo imaging is helpful for this because blood products in many stages of evolution will appear to have increased signal intensity on these sequences.



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Fig. 6A. Abruption versus placenta previa in patient at 30 weeks' gestational age with placenta previa, bleeding, and pain. Because placenta previa typically does not cause pain but abruption does, clinical question was how large a retroplacental clot was present. With large abruption, plan was to deliver immediately. Transabdominal sagittal sonogram of lower uterine segment shows placenta previa (p) with subtle increase of echogenicity in clot (arrow) above endocervical canal (arrowheads).

 


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Fig. 6B. Abruption versus placenta previa in patient at 30 weeks' gestational age with placenta previa, bleeding, and pain. Because placenta previa typically does not cause pain but abruption does, clinical question was how large a retroplacental clot was present. With large abruption, plan was to deliver immediately. Sagittal T1-weighted MR image (TR/TE, 137/4.1; field of view, 240 x 320; matrix, 128 x 256; flip angle, 80°; acquisition time, 17 sec) obtained immediately after sonogram shows to better advantage small clot (solid arrow) above internal os (open arrow), with most of placenta (P) well attached. Finding allowed patient to be treated expectantly.

 


Intraamniotic Bleeding
Top
Introduction
Hemorrhage Related to the...
Intraamniotic Bleeding
Umbilical Cord Hematoma
Bleeding Within the Fetus
Intracerebral Bleeding
Fetal Abdominopelvic Hemorrhage
Conclusion
References
 
Any hematoma affecting the intrauterine membranes can dissect through the amnion and extend into the amniotic cavity. Primary intraamniotic bleeding occurs most often after trauma. Of all traumas, abdominal trauma puts the patient most at risk of bleeding. No adverse effects to the fetus have been documented in association with intraamniotic bleeding. If intraamniotic bleeding has occurred, amniocentesis can yield dark brownish or green fluid caused by blood degradation products (Fig. 7).



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Fig. 7. Samples of amniotic fluid taken during genetic amniocentesis. Normal amniotic fluid (left) is clear bright yellow. Dark green or brown amniotic fluid (right) indicates blood degradation products caused by prior bleeding. Latter sample was obtained from patient in Figure 3A,3B. Level of {alpha}-fetoprotein in amniotic fluid may be elevated as a result of bleeding.

 

Amniocentesis is the most frequently performed procedure associated with bleeding in the pregnant patient. Intraamniotic bleeding has been reported in 100% of patients scanned immediately after transplacental amniocentesis [5]. The amount of bleeding is less when the placenta is avoided. After cessation of active bleeding, strands of echogenic material representing fibrin strands can be seen in the amniotic cavity (Fig. 8A). Clotted blood may form masses that mimic fetal anomalies (Fig. 8B). Intraamniotic fibrin strands must be differentiated from synechiae. A variable appearance of the fibrin masses or strands on successive examinations will help establish the diagnosis. After amniocentesis, the hematomas usually resolve in 3-10 weeks [5].



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Fig. 8A. Fibrin strands seen immediately after genetic amniocentesis at 17 weeks' gestational age. Transabdominal sonogram shows thin wispy membrane floating in amniotic fluid (arrow). Immediately before amniocentesis, fetal sonogram (not shown) did not show any intraamniotic membranes.

 


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Fig. 8B. Fibrin strands seen immediately after genetic amniocentesis at 17 weeks' gestational age. Sagittal sonogram of fetus reveals round echogenic mass (arrow) anterior to fetal abdomen (A); mass was caused by bleeding and clot formation but mimics anterior abdominal wall mass. Fibrin strands resolve on follow-up and should not be confused with fetal masses, amniotic band syndrome, or synechiae.

 

Echogenic particles in the amniotic fluid result directly from bleeding (Fig. 9A). When the fetus swallows blood, a mass in the stomach may be seen, as has been reported in 1.5% of sonographic studies performed after amniocentesis [6] (Fig. 9B). Less commonly, hyperechoic bowel will be seen (Fig. 10).



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Fig. 9A. Intraamniotic bleeding and gastric pseudomass in fetus at 21 weeks' gestational age, 2 weeks after transplacental amniocentesis. Transverse transabdominal sonogram shows echogenic particles floating in amniotic fluid (arrow) that were not present before amniocentesis. Until third trimester, echogenic particles in amniotic fluid should raise possibility of bleeding. Later in pregnancy, particles are most commonly the result of shed epithelial cells (vernix caseosa).

 


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Fig. 9B. Intraamniotic bleeding and gastric pseudomass in fetus at 21 weeks' gestational age, 2 weeks after transplacental amniocentesis. Transverse sonogram of fetal abdomen shows echogenic material (arrow) in stomach that results from fetus swallowing echogenic blood particles that resulted from recent amniocentesis. Gastric pseudomasses resolve on follow-up examination. To our knowledge, no gastric neoplasms have been reported on prenatal sonography.

 


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Fig. 10. Echogenic fetal bowel at 15 weeks' gestational age in 33-year old woman with vaginal bleeding. Sonogram revealed subchorionic hemorrhage (not shown). Sagittal scan through fetal abdomen reveals hyperechoic loops of bowel (arrow) as echogenic as adjacent bone. Cytomegalovirus titers and karyotype were normal, and findings of prenatal screening for cystic fibrosis were negative. Normal bowel echotexture was seen on follow-up 2 weeks later (not shown).

 


Umbilical Cord Hematoma
Top
Introduction
Hemorrhage Related to the...
Intraamniotic Bleeding
Umbilical Cord Hematoma
Bleeding Within the Fetus
Intracerebral Bleeding
Fetal Abdominopelvic Hemorrhage
Conclusion
References
 
Most umbilical cord hematomas are iatrogenic, resulting mainly from amniocentesis and percutaneous umbilical blood sampling. A large hematoma is more likely to have hemodynamic consequences for the fetus and to be associated with a worse prognosis.

Cord hematomas initially appear as echogenic masses, with progressive loss of echogenicity over time, followed by resorption (Fig. 11). They are most often seen near the cord insertion into the fetal abdomen or the placental insertion site. Cord hematoma must be differentiated from anterior abdominal wall defects and placental masses.



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Fig. 11. Umbilical cord hematoma immediately after amniocentesis at 17 weeks' gestational age. Gray-scale image of color Doppler sonogram of umbilical cord shows echogenic mass (arrows) in umbilical cord deviating vessels. Normal flow was seen in umbilical arteries and vein. Finding was not present before amniocentesis.

 


Bleeding Within the Fetus
Top
Introduction
Hemorrhage Related to the...
Intraamniotic Bleeding
Umbilical Cord Hematoma
Bleeding Within the Fetus
Intracerebral Bleeding
Fetal Abdominopelvic Hemorrhage
Conclusion
References
 
Bleeding isolated to the fetus is rare. It may result from a primary fetal blood dyscrasia, a vascular malformation, trauma, maternal bleeding disorders, anticoagulants, or antiepileptic drugs. The cause is often undetermined.


Intracerebral Bleeding
Top
Introduction
Hemorrhage Related to the...
Intraamniotic Bleeding
Umbilical Cord Hematoma
Bleeding Within the Fetus
Intracerebral Bleeding
Fetal Abdominopelvic Hemorrhage
Conclusion
References
 
Intracerebral hemorrhage usually portends a poor prognosis; many of the cases reported in the literature resulted in fetal demise [7]. Intracerebral bleeding remains a rare occurrence in utero. MR imaging is more sensitive than sonography in detecting and defining the extent of such bleeding [8] (Figs. 12A,12B,12C,12D and 13A,13B,13C).



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Fig. 12A. Cortical hemorrhage in patient examined at 16 weeks' gestational age. Transabdominal oblique coronal sonogram of fetal head shows mild ventriculomegaly with choroid plexus in dependent location. Margins of lateral ventricular walls are irregular (arrows). Finding suggests destructive process in periventricular cortical tissue.

 


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Fig. 12B. Cortical hemorrhage in patient examined at 16 weeks' gestational age. Coronal half-Fourier single-shot turbo spin-echo MR images (TEeff, 60; field of view, 245 x 280; matrix, 192 x 256; flip angle, 130°; acquisition time, 420 msec) show destruction of brain tissue in right frontal lobe (arrows, B) with focal area of low signal intensity in right frontal lobe (arrow, C). Because of use of ultrafast sequences, no fetal or maternal sedation was necessary.

 


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Fig. 12C. Cortical hemorrhage in patient examined at 16 weeks' gestational age. Coronal half-Fourier single-shot turbo spin-echo MR images (TEeff, 60; field of view, 245 x 280; matrix, 192 x 256; flip angle, 130°; acquisition time, 420 msec) show destruction of brain tissue in right frontal lobe (arrows, B) with focal area of low signal intensity in right frontal lobe (arrow, C). Because of use of ultrafast sequences, no fetal or maternal sedation was necessary.

 


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Fig. 12D. Cortical hemorrhage in patient examined at 16 weeks' gestational age. Axial fast T1-weighted MR image (TR/TE, 137/4.1; field of view, 240 x 320; matrix, 128 x 256; flip angle, 80°) reveals extraaxial high and low signal intensity (arrow), consistent with blood products. Pregnancy was terminated. (Reprinted from [9])

 


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Fig. 13A. Extraaxial bleeding in fetus at 20 weeks' gestational age. Axial sonogram of fetal head reveals extraaxial collection of blood (solid arrow) in posterior fossa, pushing and deforming cerebellum (c). Dependent echoes (open arrow) are suggestive of clot.

 


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Fig. 13B. Extraaxial bleeding in fetus at 20 weeks' gestational age. Corresponding axial half-Fourier single-shot turbo spin-echo MR image of fetal head (TEeff, 60; field of view, 225 x 300; matrix, 192 x 256; flip angle, 130°; acquisition time, 13 sec) again show extraaxial collection in posterior fossa (solid arrow) extending superiorly, with hypointense focus caused by clot or calcification (open arrow). This is intratentorial bleeding.

 


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Fig. 13C. Extraaxial bleeding in fetus at 20 weeks' gestational age. Coronal MR image of fetal head also shows subarachnoid blood (curved arrows). Note midline superior sagittal sinus (straight arrow). Postnatal imaging (not shown) showed almost complete resolution of hematoma.

 


Fetal Abdominopelvic Hemorrhage
Top
Introduction
Hemorrhage Related to the...
Intraamniotic Bleeding
Umbilical Cord Hematoma
Bleeding Within the Fetus
Intracerebral Bleeding
Fetal Abdominopelvic Hemorrhage
Conclusion
References
 
Fetal abdominopelvic hemorrhage may be primary and may secondarily involve any mass, the most frequent being adrenal (Fig. 14A,14B,14C) and ovarian (Fig. 15) lesions. A lesion presenting in a suprarenal location warrants follow-up. Neuroblastomas present many features similar to those of hematomas, and resolution over time suggests a benign cause.



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Fig. 14A. Neuroblastoma with hemorrhage in fetus at 34 weeks' gestational age referred for evaluation of right suprarenal mass. Coronal sonogram of fetal abdomen shows complex mass (arrow) above right kidney (arrowheads). No normal adrenal tissue is identified.

 


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Fig. 14B. Neuroblastoma with hemorrhage in fetus at 34 weeks' gestational age referred for evaluation of right suprarenal mass. Sagittal oblique half-Fourier single-shot turbo spin-echo MR image of fetus (TR/TEeff, xx/64; field of view, 320 x 320; matrix, 192 x 256; flip angle, 130°; acquisition time, 13 sec) shows hyperintense well-demarcated lesion (arrow) above right kidney (arrowheads).

 


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Fig. 14C. Neuroblastoma with hemorrhage in fetus at 34 weeks' gestational age referred for evaluation of right suprarenal mass. Axial T1-weighted MR image (TR/TE, 132/4; field of view, 297 x 340; matrix, 112 x 256; flip angle, 80°; acquisition time, 16 sec) through fetal abdomen shows clear fluid-fluid level (straight arrow) compatible with intracystic hemorrhage. Cyst is of mixed signal intensities, with higher signal intensity debris in dependent portion of cyst (curved arrow) consistent with blood degradation products. CT scan after birth (not shown) showed hemorrhagic adrenal lesion. Because of increasing size of lesion after birth, excision was performed when infant was 3 months old. Histology revealed hemorrhagic neuroblastoma.

 


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Fig. 15. Ovarian cyst in female fetus at 34 weeks' gestational age. Coronal sonogram shows complex cystic mass (arrow) in left abdomen (s = stomach, b = bladder). Through-transmission is seen posterior to cyst. On follow-up scans (not shown), cyst size remained the same but hematoma in cyst decreased in size. Excision was performed when infant was 3 months old, and pathology revealed intrauterine ovarian torsion.

 


Conclusion
Top
Introduction
Hemorrhage Related to the...
Intraamniotic Bleeding
Umbilical Cord Hematoma
Bleeding Within the Fetus
Intracerebral Bleeding
Fetal Abdominopelvic Hemorrhage
Conclusion
References
 
This pictorial essay illustrates the sonographic and MR imaging findings of prenatal hemorrhage. Awareness of the various manifestations of hemorrhage in pregnancy is important for patient counseling and treatment.


References
Top
Introduction
Hemorrhage Related to the...
Intraamniotic Bleeding
Umbilical Cord Hematoma
Bleeding Within the Fetus
Intracerebral Bleeding
Fetal Abdominopelvic Hemorrhage
Conclusion
References
 

  1. Nyberg DA, Cyr DR, Mack LA, Wilson DA, Shuman WP. Sonographic spectrum of placental abruption. AJR 1987;148:161 -164[Abstract/Free Full Text]
  2. Goldstein SR, Subramanyam BR, Raghavendra BN, Horii SC, Hilton S. Subchorionic bleeding in threatened abortion: sonographic findings and significance. AJR 1983;141:975 -978[Abstract/Free Full Text]
  3. Bennett GL, Bromley B, Lieberman E, Benacerraf BR. Subchorionic hemorrhage in first-trimester pregnancies: prediction of pregnancy outcome with sonography. Radiology 1996;200 : 803-806[Abstract/Free Full Text]
  4. Nyberg DA, Mack LA, Benedetti TJ, Cyr DR, Schuman WP. Placental abruption and placental hemorrhage: correlation of sonographic findings with fetal outcome. Radiology 1987;164:357 -361[Abstract/Free Full Text]
  5. Chinn DH, Towers CV, Beeman RG, Miller EI. Sonographically demonstrated intra-amniotic hemorrhage following transplacental genetic amniocentesis. J Ultrasound Med 1990; 9:495 -501[Abstract]
  6. Daly-Jones E, Sepulveda W, Hollingsworth J, Fisk NM. Fetal intraluminal gastric masses after second trimester amniocentesis. J Ultrasound Med 1994;13:963 -966[Abstract]
  7. Fogarty K, Cohen HL, Haller JO. Sonography of fetal intracranial hemorrhage: unusual causes and a review of the literature. J Clin Ultrasound 1989;17:366 -370[Medline]
  8. Levine D, Barnes PD, Madsen JR, Abbott J, Mehta T, Edelman RR. Central nervous system abnormalities assessed with prenatal magnetic resonance imaging. Obstet Gynecol 1999;94:1011 -1019[Medline]
  9. Levine D, Barnes PD, Madson JR, et al. Fetal CNS anomalies revealed on ultrafast MR imaging. AJR 1999;172:813 -818[Free Full Text]

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