Ultrasound-Detected Subchorionic

Hemorrhage and the Obstetric Implications

Shayna M. Norman, MD, Anthony O. Odibo, MD, MSCE, George A. Macones,
Jeffrey M. Dicke, MD, James P. Crane, MD, and Alison G. Cahill, MD, MSCI
OBJECTIVE: To estimate the association between the
ultrasonographic diagnosis of subchorionic hemorrhage
and adverse pregnancy outcomes.
METHODS: This was a retrospective cohort study of all
consecutive women undergoing routine ultrasonography
before 22 weeks with a singleton gestation at one institution from 1994 to 2008. Presence or absence of subchorionic hemorrhage defined the two study groups. The
primary outcomes were abruption, intrauterine growth
restriction defined as birth weight less than the 10th
percentile, and nonanomalous intrauterine fetal demise
after 20 weeks. Secondary outcomes included preeclampsia, preterm premature rupture of membranes,
and preterm delivery before 37 weeks and before 34
weeks of gestation. Univariable, bivariate, and multiple
logistic regression analyses were performed.
RESULTS: Of the 63,966 women in the patient population, 1,081 had subchorionic hemorrhage (1.7%).
Women with a subchorionic hemorrhage were at increased risk of abruption (n432, 3.6% compared with
0.6%, adjusted odds ratio 2.6, 95% confidence interval
1.8 3.7) and of preterm delivery (n6,601, 15.5% compared with 10.5%, adjusted odds ratio 1.3, 95% confidence interval 1.11.5), even after adjusting for bleeding during pregnancy, chronic hypertension, body
mass index, race, diabetes mellitus, tobacco use, and
previous preterm delivery.
CONCLUSION: Women with ultrasound-detected subchorionic hemorrhage before 22 weeks of gestation are
at increased risk of placental abruption and preterm
From Department of Obstetrics and Gynecology, Washington University, St.
Louis, Missouri.
Presented as a poster at the annual meeting of the Society of Maternal Fetal
Medicine, February 4, 2010, Chicago, Illinois.
Corresponding author: Shayna M. Norman, MD, 4911 Barnes Jewish Hospital
Plaza, St. Louis, MO 63110; e-mail: normans@wudosis.wustl.edu.
Financial Disclosure
The authors did not report any potential conflicts of interest.
2010 by The American College of Obstetricians and Gynecologists. Published
by Lippincott Williams & Wilkins.
ISSN: 0029-7844/10

VOL. 116, NO. 2, PART 1, AUGUST 2010

MD, MSCE,

delivery but are not at increased risk of other adverse

pregnancy outcomes.
(Obstet Gynecol 2010;116:3115)

LEVEL OF EVIDENCE: II

he detection of subchorionic hemorrhage is a

relatively common finding on ultrasound examinations. The two largest studies to date report an
incidence of subchorionic hemorrhage of 1.3% to
3.1%.1,2 However, the clinical outcomes associated
with sonographically detected subchorionic hemorrhage are not well-established.
In the past, studies have found opposing results.
Some investigators have reported an association between subchorionic hemorrhage and abruption, preterm delivery, intrauterine growth restriction (IUGR),
or intrauterine fetal death, whereas others have found
no association between subchorionic hemorrhage and
these outcomes.13 These studies have mainly focused
on the finding of subchorionic hemorrhage in the first
trimester, making their findings only generalizable to
patients who undergo a first-trimester ultrasound examination and are potentially biased by the indication
for ultrasonography in the first place, such as bleeding. Conflicting data and small sample sizes have
ultimately left clinicians unable to confidently counsel
patients when subchorionic hemorrhage is detected
on routine ultrasound examination.
This study aims to estimate the association between the ultrasonographic diagnosis of subchorionic
hemorrhage and adverse pregnancy outcomes, including placental abruption, IUGR, and intrauterine
fetal death.

MATERIALS AND METHODS

We conducted a retrospective cohort study of all
viable, singleton pregnancies undergoing routine ultrasound anatomic survey between 17 and 22 weeks
of gestation during the 14-year study period from

OBSTETRICS & GYNECOLOGY

311

1994 to 2008 at Washington University in St. Louis

Medical Center. Before initiation of the study, approval was obtained from the Washington University
human research protection board. The Washington
University prenatal diagnosis database was created in
1990 and has gathered extensive information on all
women who have undergone ultrasound evaluation
(including demographics, medical, obstetric, and social history, indication for examination, and ultrasound findings). Dedicated pregnancy outcome coordinators obtained complete pregnancy outcome data
for women undergoing ultrasound evaluation in an
ongoing, prospective manner, contemporaneously
with delivery admission, and by record acquisition
and physician contact in the rare event of delivery at
an out-of-network hospital or if delivery admission
was missed. Included in this analysis are only those
patients with complete follow-up data.
Pregnancies were dated by a womans last menstrual period if that date was within 7 days of a firsttrimester ultrasound examination or within 10 days of a
second-trimester ultrasound examination. Pregnancies
were dated by ultrasonography if the last menstrual
period was unknown or if the ultrasound dating was
outside the aforementioned parameters. At the time of
anatomic survey, placentas were evaluated as a routine
part of the study using the American Institute of Ultrasound in Medicine guidelines.4 All ultrasound examinations were performed by full-time registry of diagnostic
medical ultrasonographers credentialed in obstetrics
and gynecology. Final diagnostic interpretations were
made by maternalfetal medicine attending physicians.
Presence of subchorionic hemorrhage, defined as a
retroplacental, hypoechoic region, of any size and any
location was included in the study (Fig. 1).5
Presence or absence of subchorionic hemorrhage, determined dichotomously by the attending

physician performing the final ultrasound interpretation, identified the two study groups. The primary
outcomes of the study were placental abruption defined clinically by the attending physician at the time
of delivery, IUGR defined as birth weight less than
the 10th percentile based on the Alexander growth
standard,6 and intrauterine fetal death after 20 weeks
of gestation. Fetuses with major congenital anomalies
were excluded from the analysis of intrauterine fetal
death.5 Secondary outcomes studied were preeclampsia, defined using American College of Obstetricians
and Gynecologists criteria (the College), for which
both mild and severe preeclampsia were included,
preterm premature rupture of membranes (PROM),
also defined using the College criteria, and preterm
delivery before 37 weeks of gestation as well as before
34 weeks of gestation.7,8 Only patients who delivered
after 20 weeks of gestation were included in our
analysis. Baseline characteristics were compared between the two study groups (women with subchorionic hemorrhage and those without). Continuous
variables were compared using the Student t and
Mann-Whitney U tests, and categorical variables were
compared using the 2 and Fisher exact test as
appropriate. Stratified analyses were used to identify
potentially confounding factors. Incidence, relative
risks and 95% confidence intervals (CI) were calculated for each of the primary and secondary outcomes. Bleeding during the first trimester or any time
before the anatomy scan was considered in subgroup
analyses to distinguish between a symptomatic patient
and one in whom the finding of subchorionic hemorrhage was incidental. Additionally, analyses of the
preterm delivery outcomes were further explored,
excluding cases of placental abruption. The results of
the univariable and stratified analyses were used to
select factors for our final multivariable models for the

Fig. 1. A. Subchorionic hemorrhage detected in the first trimester

in a twin gestation. Arrows indicate subchorionic hemorrhage. B.
Subchorionic hemorrhage detected in the second trimester at a
routine anatomic survey in a singleton gestation. Arrows indicate
subchorionic hemorrhage.
Norman. Subchorionic Hemorrhage
and Obstetric Implications. Obstet
Gynecol 2010.

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outcomes. Backward step-wise selection was used to

reduce the number of variables in the model by
assessing the magnitude of change in the effect size of
subchorionic hemorrhage and other risk covariates.
Differences in the explanatory models were tested
using the likelihood ratio test or Wald test.9 Only
variables that were statistically significant were included in the final models. All statistical analyses were
completed using STATA software package, version
10, special edition (College Station, TX).

RESULTS
Of 72,373 women, 63,966 had complete follow-up
data and therefore were available for this analysis.
Subchorionic hemorrhage was identified in 1,081
(1.7%) women.
Baseline characteristics of the two study groups
are provided in Table 1. Women with subchorionic
hemorrhage are more likely to be advanced maternal
Table 1. Characteristics of Women With a
Ultrasonographically Identified
Subchorionic Hemorrhage Compared
With Those Without
Subchorionic Subchorionic
Hemorrhage Hemorrhage
Present,
Absent,
n1,081
n62,885
Age (y)
Advanced maternal
age (n19,029)
Gravidity (number
of pregnancies)
Parity (number of
deliveries)
Body mass index (kg/m2)
African American
(n13,248)
Previous preterm
delivery
(n3,459)
Tobacco use (n7,191)
Alcohol use (n12,445)
Bleeding (n3,661)*
Chronic hypertension
(n1,535)
Gestational diabetes
(n1,119)
Pregestational
diabetes (n1,114)
Gestational age at
ultrasound
examination (wk)
Gestational age at
delivery (wk)

31.6 5.9
35.5

30.1 6.3
29.6

.01
.01

3.1 1.8

2.7 1.6

.01

1.3 1.3

1.0 1.1

.01

23.5 8.0
13.9

24.6 9.1
20.8

.01
.01

7.7

5.4

.01

9.6
21.0
32.5
2.7

11.3
19.6
5.3
2.4

.07
.23
.01
.54

2.1

1.7

.34

2.2

1.7

.23

17.7 1.9

18.4 1.8

.01

37.5 4.6

38.2 4.6

.01

Data are meanstandard deviation or % unless otherwise specified.

* Bleeding before 20 weeks of gestation.

VOL. 116, NO. 2, PART 1, AUGUST 2010 Norman et al

age, with higher gravidity and parity, lower body

mass index, and of nonAfrican-American race.
Women with subchorionic hemorrhage also were
more likely to have a history of previous preterm
birth and were more likely to have reported bleeding
during the pregnancy before their ultrasound evaluation. Women with subchorionic hemorrhage also
underwent ultrasound examinations at an earlier gestational age, on average, compared with those without
subchorionic hemorrhage (17.7 weeks compared with
18.4 weeks).
Women with subchorionic hemorrhage were
found to have a statistically significant increased risk
of abruption (n432, 3.6% compared with 0.6%,
adjusted odds ratio [aOR] 2.6, 95% CI 1.8 3.7,
P.01), even after adjusting for bleeding, chronic
hypertension, pregestational diabetes, tobacco use,
and previous preterm birth (Table 2). Additionally,
presence of a subchorionic hemorrhage was associated with an increased risk of abruption regardless of
whether there had been bleeding before the ultrasound examination (ie, symptomatic; aOR 1.6, 95%
CI 1.0 2.7), or if subchorionic hemorrhage was an
incidental finding (aOR 5.0, 95% CI 3.0 8.3).
The risks of preterm delivery before 37 weeks of
gestation (n6601, 15.5% compared with 10.5%,
aOR 1.3, 95% CI 1.11.5, P.01) and before 34
weeks of gestation (n1774, 5.3% compared with
2.8%, aOR 1.5, 95% CI 1.12.0, P.01) were significantly higher in women with subchorionic hemorrhage after adjusting for previous preterm birth,
bleeding, and tobacco use (Table 3). Chronic hypertension, body mass index, race, and diabetes mellitus
did not remain significant in the final models. Additionally, the association between subchorionic hemorrhage and risk of preterm delivery before 37 and 34
weeks of gestation remained even after excluding
cases of abruption (preterm delivery less than 37
weeks: 14.5% compared with 10.4%, aOR 1.5, 95%
CI 1.21.8, P.01; preterm delivery less than 34
weeks: 4.2% compared with 2.7%, aOR 1.7, 95% CI
1.32.4, P.01). Symptomatic bleeding did not have
an impact on the risk of preterm delivery or any of the
other outcomes of interest. There was no statistically
significant association between presence of subchorionic hemorrhage and preterm PROM (n1,484,
4.1% compared with 2.3%, aOR 1.3, 95% CI 1.0 1.8,
P.07), IUGR (n8,159, 13.0% compared with
13.1%, aOR 1.1, 95% CI 0.9 1.4, P.59), intrauterine
fetal death (n445, 1.3% compared with 0.8%, aOR
1.4, 95% CI 0.8 3.1, P.21), or preeclampsia
(n4,683, 6.4% compared with 7.5%, aOR 0.8, 95%
CI 0.6 1.1, P.18).

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Table 2. Effect of Subchorionic Hemorrhage on the Risk for Abruption, Intrauterine Growth Restriction,
and Intrauterine Fetal Demise

Abruption (n432)
Symptomatic (n145)
Not symptomatic (n287)
Intrauterine growth restriction
(n8,159)
Intrauterine fetal demise (n445)

Subchorionic
Hemorrhage
Present (n1,081, %)

Subchorionic
Hemorrhage
Absent (n62,885, %)

Relative Risk
(95% CI)

Adjusted
Odds Ratio
(95% CI)

3.6
6.1
2.4
13.0

0.6
3.8
0.5
13.1

5.6 (4.07.7)
1.6 (1.02.5)
5.1 (3.28.3)
1.0 (0.81.2)

2.6 (1.83.7)*
1.6 (1.02.7)
5.0 (3.08.3)
1.1 (0.91.4)

.01
.04
.01
.59

1.3

0.8

1.7 (1.03.0)

1.4 (0.83.1)

.21

CI, confidence interval

* Adjusted for bleeding, chronic hypertension, preexisting diabetes, tobacco use, and previous preterm birth.

Bleeding before 20 weeks of gestation.

Adjusted for previous preterm birth and tobacco use.

Adjusted for advanced maternal age, body mass index, African-American race, previous preterm birth, bleeding, chronic
hypertension, gestational diabetes, tobacco use, and alcohol use.

Adjusted for African-American race, bleeding, chronic hypertension, pregestational diabetes, and tobacco use.

DISCUSSION
We found that the detection of a subchorionic hemorrhage during routine second-trimester ultrasonography
was associated with a more than twofold increased risk
of placental abruption, regardless of whether the woman
reported bleeding in the early half of pregnancy. We
also identified that women with subchorionic hemorrhage are at increased risk of preterm delivery. In
contrast, we did not find evidence for an increased risk
of IUGR, intrauterine fetal death, preterm PROM, or
preeclampsia in women with subchorionic hemorrhage
compared with those without. Our findings represent
new, more robust information regarding the risks associated with the common clinical entity, subchorionic
hemorrhage, compared with the existing data in the
published literature.
After a few early observational reports,10,11 Ball et
1
al conducted a case control study that examined

pregnancy outcomes in 238 individuals found to have

subchorionic hemorrhage on first-trimester scan. This
study found ultrasonically detected subchorionic
hemorrhage to be associated with an increased risk of
subsequent placental abruption and preterm labor.
The study by Ball et al1 found no increased risk of
IUGR in those with subchorionic hemorrhage, but it
did find a statistically significant association with
intrauterine fetal death that was related to increasing
size of the hemorrhage. Later, among more observational studies,3,1215 Nagy et al2 studied 187 individuals
with subchorionic hemorrhage compared with 6,488
women in the control group and found an increased
risk of abruption, IUGR, and preterm delivery, but
the study did not demonstrate an association with
intrauterine fetal death. Size and location of hematoma did not correlate with any adverse pregnancy
outcomes.

Table 3. Effect of Subchorionic Hemorrhage on the Risk for Preterm Delivery, Preeclampsia, and
Preterm Premature Rupture of Membranes

Preterm delivery less than 37

wk of gestation (n6,601)
Preterm delivery less than 34
wk of gestation (n1,774)
Preeclampsia (n4,683)
Preterm premature rupture of
membranes (n1,484)

Subchorionic
Hemorrhage
Present (n1,081, %)

Subchorionic
Hemorrhage
Absent (n62,885, %)

Relative Risk
(95% CI)

Adjusted Odds
Ratio (95% CI)

15.5

10.5

1.5 (1.31.7)

1.3 (1.11.5)*

.01

5.3

2.8

1.9 (1.52.5)

1.5 (1.12.0)*

.01

6.4
4.1

7.5
2.3

0.8 (0.71.1)
1.8 (1.32.4)

0.8 (0.61.1)
1.3 (1.01.8)

.18
.07

CI, confidence interval.

* Adjusted for bleeding, previous preterm birth, and tobacco use.

Adjusted for advanced maternal age, body mass index, African-American race, chronic hypertension, pregestational diabetes, and
previous preterm birth.

Adjusted for parity, African-American race, previous preterm birth, bleeding, and tobacco use.

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By studying a cohort of unselected patients undergoing routine, standard-of-care, second-trimester

anatomic survey, we were able to more accurately
assess the incidence of subchorionic hemorrhage. Our
larger sample also allowed us to estimate the associated risk of many less-frequent adverse pregnancy
outcomes with the detection of subchorionic hemorrhage. The detailed information available for the
patients in our cohort, including demographics, history, and pregnancy outcomes, allowed us to identify
many associated outcomes and adjust for potential
confounders. Finally, by identifying our cohort by
those undergoing a routine second-trimester anatomic
survey, we are able to avoid the selection bias inherent in selecting based on first-trimester ultrasound
examinations, allowing our results to be applied to the
general obstetric population. Despite the strengths of
our study, there are some limitations that must be
considered as well. Previous studies have attempted
to adjust for size or location of subchorionic hemorrhage, but we were unable to do so because only the
presence or absence of subchorionic hemorrhage was
most frequently recorded.1,5,11 However, although we
did not evaluate or adjust for these features, it is worth
noting that the size of the hemorrhage was large
enough to be clinically observed, further improving
our generalizability. Additionally, approximately 11%
of the potential cohort lacked outcome data and could
not be included in this analysis, creating the potential
for selection bias. However, patients who lacked
follow-up information did not differ from those analyzed on baseline or exposure characteristics, making
the potential impact of this on the result minimal.
Last, as is the case with all retrospective and many
prospective studies that investigate preterm PROM as
an outcome, there may be some misclassification with
regard to concomitant preterm labor that cannot be
accounted for with statistics.
We found that patients with an ultrasound-detected subchorionic hemorrhage at the time of routine
anatomic survey have an increased risk of placental
abruption and preterm birth, corroborating earlier
findings in smaller studies with selected patient populations. Although there is currently no prevention or
treatment for either of these outcomes, patients with
an identified subchorionic hemorrhage could be

VOL. 116, NO. 2, PART 1, AUGUST 2010 Norman et al

counseled to report early with any bleeding or signs

or symptoms of preterm labor because of their increased risk. Conversely, patients can be reassured
based on our findings that the identification of subchorionic hemorrhage does not confer an increased
risk of IUGR, intrauterine fetal death, preeclampsia,
or preterm PROM.
REFERENCES
1. Ball RH, Ade CM, Schoenborn JA, Crane JP. The clinical
significance of ultrasonographically detected subchorionic
hemorrhages. Am J Obstet Gynecol 1996;174:996 1002.
2. Nagy S, Bush M, Stone J, Lapinski RH, Gardo S. Clinical
significance of subchorionic and retroplacental hematomas
detected in the first trimester of pregnancy. Obstet Gynecol
2003;103:94 100.
3. Maso G, DOttavio G, De Seta F, Sartore A, Piccoli M,
Mandruzzato G. First-trimester intrauterine hematoma and
outcome of pregnancy. Obstet Gynecol 2005;105:339 44.
4. American Institute of Ultrasound in Medicine. AIUM practice
guideline for the performance of obstetric ultrasound examinations. J Ultrasound Med 2010;29:166 72.
5. Callen PW. Ultrasonography in obstetrics and gynecology,
2008. Philadelphia (PA): Saunders; 2008.
6. Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A
United States national reference for fetal growth. Obstet
Gynecol 1996;87:163 8.
7. Diagnosis and management of preeclampsia and eclampsia.
ACOG Practice Bulletin No. 33. American College of Obstetricians and Gynecologists. Obstet Gynecol 2002;99:159 67.
8. Premature rupture of membranes. ACOG Practice Bulletin
No. 80. American College of Obstetricians and Gynecologists.
Obstet Gynecol 2007;109:100719.
9. Hosmer D, Lemeshow S. Applied Logistic Regression, 2000.
New York (NY): John Wiley & Sons; 2000.
10. Abu-Yousef MM, Bleicher JJ, Williamson RA, Weiner CP.
Subchorionic hemorrhage: sonographic diagnosis and clinical
significance. Am J Radiology 1987;149:737 40.
11. Bennett GL, Bromley B, Lieberman E, Benacerraf BR. Subchorionic hemorrhage in first-trimester pregnancies: prediction of pregnancy outcome with sonography. Radiology 1996;
200:803 6.
12. Sharma G, Kalish RB, Chasen ST. Prognostic factors associated with antenatal subchorionic echolucencies. Am J Obstet
Gynecol 2003;189:994 6.
13. Leite J, Ross P, Rossi AC, Jeanty P. Prognosis of very large
first-trimester hematomas. J Ultrasound Med 2006;25:14415.
14. Johns J, Hyett J, Jauniaux E. Obstetric outcome after threatened miscarriage with and without a hematoma on ultrasound.
Ultrasound Obstet Gynecol 2003;102:4837.
15. Signore CC, Sood AK, Richards DS. Second-trimester vaginal
bleeding: correlation of sonographic findings with perinatal
outcome. Am J Obstet Gynecol 1998;178:336 40.

Subchorionic Hemorrhage and Obstetric Implications

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