DOI:10.2214/AJR.05.0152
AJR 2006; 187:W350-W356
© American Roentgen Ray Society
Diagnosis and Characterization of Fetal Sacrococcygeal Teratoma with Prenatal MRI
Enrico Danzer1,
Anne M. Hubbard2,
Holly L. Hedrick1,
Mark P. Johnson1,
R. Douglas Wilson1,
Lori J. Howell1,
Alan W. Flake1 and
N. Scott Adzick1
1 The Center for Fetal Diagnosis and Treatment, Department of Radiology, The
Children's Hospital of Philadelphia, Philadelphia, PA 19104-4399.
2 University of Nebraska Medical Center, 981045 Nebraska Medical Center, Omaha,
NE 68199-1045.
Received January 30, 2005;
accepted after revision April 11, 2005.
Address correspondence to A. M. Hubbard
(amhubbard{at}unmc.edu).
WEB
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Abstract
OBJECTIVE. The purpose of this study was to determine whether
prenatal MRI provides additional information about fetal sacrococcygeal
teratoma compared with prenatal sonography.
MATERIALS AND METHODS. Twenty-two pregnant women with fetal
sacrococcygeal teratoma underwent prenatal MRI (mean gestational age, 23
weeks). The size, location, mass characteristics, and compressive effects of
the tumors were determined and correlated with sonography and postnatal
findings.
RESULTS. Based on the MRI findings, the following American Academy
of Pediatrics, Surgical Section classifications were assigned: type I in six
patients, type II in 12, and type III in four. No type IV tumors were found.
The sacrococcygeal teratoma appeared entirely cystic in five fetuses,
microcystic in one, mixed cystic and solid in 12, and solid in four. The
diagnosis of sacrococcygeal teratoma was accurate in all cases assessed at our
center using both MRI and sonography. Two additional patients initially
referred with the diagnosis of sacrococcygeal teratoma had a different
diagnosis at reevaluation at our institution (healthy, n = 1;
myelomeningocele, n = 1). MRI was superior to sonography for
detecting displacement of the colon (n = 11), urinary tract
dilatation (n = 9), hip dislocation (n = 4), intraspinal
extension (n = 2), and vaginal dilation (n = 1). In fetuses
with sacrococcygeal teratoma types II and III, MRI better showed the cephalic
extent of the tumor compared with sonography. MRI findings were confirmed at
surgery or autopsy in all patients. Three fetuses with high output cardiac
physiology underwent open fetal resection of the tumor at 21-, 24-, and
26-weeks' gestational age with two surviving.
CONCLUSION. Our results show that ultrafast fetal MRI is a useful
adjunct to the prenatal evaluation of fetal sacrococcygeal teratoma. Compared
with sonography, MRI more accurately characterized the intrapelvic and
abdominal extent of the tumors and provided more information on compression of
adjacent organs. The additional anatomic resolution provided by MRI resulted
in more accurate prenatal counseling and improved preoperative planning for
surgical resection.
Keywords: fetal imaging • fetal intervention • fetus • prenatal MRI • sacrococcygeal teratoma
Introduction
Although rare, sacrococcygeal teratoma is the most common tumor of the
fetus and the neonate, with a reported incidence of one in 35,000 to 40,000
live births
[1-3].
It has been defined as either a neoplasm composed of tissues from all three
germ layers or a neoplasm formed from multiple tissues foreign to the part and
lacking organ specificity [4].
These tumors arise from totipotent somatic cells
[5] that originate from the
primitive knot (Hensen's node) or caudal cell mass and escape normal inductive
influences.
The natural history of prenatally diagnosed sacrococcygeal teratoma differs
from postnatally diagnosed sacrococcygeal teratoma. Malignant degeneration,
the primary cause of death in postnatal sacrococcygeal teratoma, is rare in
utero. The high mortality rate of fetal sacrococcygeal teratoma is attributed
to tumor mass and associated dystocia, preterm labor caused by secondary
polyhydramnios, and development of hydrops and placentomegaly (secondary to
high-output cardiac failure associated with arteriovenous shunting)
[6-8].
Prenatal assessment of the fetus is critical for counseling the parents and
planning surgical options. Also, with the development of in utero treatment
for sacrococcygeal teratoma [9,
10], it is important to select
appropriate candidates for fetal surgery. Because of acoustic shadowing by the
fetal pelvic bones, sonography cannot always define the most cephalad extent
of sacrococcygeal teratoma
[11].
Prenatal MRI for evaluating uterine and fetal anatomy has improved with the
development of ultrafast MRI techniques
[12,
13]. Fetal MRI has been
successfully performed with echo-planar and RARE imaging
[13-16].
MRI offers superior anatomic resolution, regardless of fetal orientation, and
it provides an image display that is more intuitively comprehensible to the
patient and to many consulting physicians. Despite the increasing use of
prenatal MRI, to our knowledge only a few small case series have been
published comparing the advantages and disadvantages of prenatal sonography
and MRI of sacrococcygeal teratoma
[11,
17,
18]. This study compared the
diagnostic utility of prenatal MRI and transabdominal sonography for
evaluation of sacrococcygeal teratoma to determine whether MRI could provide
additional valuable clinical information.
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Fig. 1 —26-weeks' gestation fetus with type I sacrococcygeal
teratoma. Sagittal T2-weighted images show mixed solid and cystic lesion
(arrowheads) arising from coccyx (double-headed arrow). No
intrapelvic extension of tumor is seen. Urinary bladder (small arrow)
is in normal position.
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Fig. 2 —22-weeks' gestation fetus with type II sacrococcygeal
teratoma. Sagittal T2-weighted image shows large septate cystic mass
(arrowheads) arising from coccyx (double-headed arrow) with
small intrapelvic component. Urinary bladder (small arrow) is not
displaced.
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Materials and Methods
Patient Population
From March 1998 to January 2003 21 patients were diagnosed with
sacrococcygeal teratoma at our clinic. Two additional patients were referred
from another institution with the diagnosis of sacrococcygeal teratoma, but
neither was found to have sacrococcygeal teratoma at reevaluation (healthy,
n = 1; myelomeningocele, n = 1). In addition, one patient
referred for myelomeningocele was found by sonography and MRI at our center to
have sacrococcygeal teratoma type III. This patient was added to the study,
making the total number of patients 22. Prenatal evaluation included a repeat
high-resolution fetal sonogram, fetal echocardiography, and MRI to assess the
sacrococcygeal teratoma anatomy, placental size, and presence or absence of
hydrops. Fetal echocardiography and Doppler flow measurements were obtained to
assess high-output physiology. MRI was performed at a single institution by
multiple radiologists as part of clinical evaluation of a fetus with
abnormalities. The mean gestational age at MRI evaluation was 23 weeks (range,
19-33 weeks). After evaluation, all patients underwent nondirective counseling
for management options. The options included (1) termination of pregnancy if
the gestational age was less than 24 weeks; (2) standard postnatal care with
continued weekly, biweekly, or triweekly sonography and echocardiography
surveillance; and (3) fetal intervention if the fetus met intervention
criteria. This retrospective study was approved by our institutional review
board, Committees for Protection of Human Subjects (IRB #2002-8-2912).
MRI
MRI was performed with a 1.5-T magnet (Vision, Siemens Medical Solutions)
equipped with a phased-array body coil. The nonsedated mother was positioned
either supine or in a partial left lateral decubitus position. The following
imaging sequences were performed: RARE HASTE imaging (TR/effective TE,
1,100/62; flip angle, 130°; section thickness, 4-5 mm) in the sagittal,
coronal, and axial planes relative to the fetus; T1-weighted gradient-echo
fast low-angle shot (FLASH) (TR/TE, 174.9/4.4; flip angle, 65°; section
thickness, 4 mm) in the axial plane relative to the fetus; and echo-planar
free induction decay imaging (effective TR/TE, 3,900/56; flip angle, 90°;
section thickness, 4 mm) in the axial plane. For each sequence, 4-20 seconds
was needed to acquire 20 anatomic images.
All MR studies were reviewed and interpreted by the same radiologist, who
also knew the results of sonography or had the clinical information based on
outside sonography. MRI results were compared with sonography reports and
images. The presence, size, signal intensity characteristics, extent, and
compressive effects of the sacrococcygeal teratoma were determined and
correlated with findings from postnatal studies, including postmortem,
surgical, or pathologic results. Hydrops was defined as the presence of skin
edema and ascites or pericardial or pleural effusion. The presence of oligo-
or polyhydramnios was determined by calculating the amniotic fluid index. The
extent of the sacrococcygeal teratoma was classified according the American
Academy of Pediatrics, Surgical Section classification
[19]. Type I is primarily
external and has only a minimal presacral component. Type II is primarily
external but has a significant intrapelvic portion. Type III is partially
external but is predominantly intrapelvic with abdominal extension. Type IV is
located entirely within the pelvis and abdomen.
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Fig. 3A —29-weeks' gestation fetus with type III sacrococcygeal
teratoma. Sagittal T2-weighted image shows oligohydramnios. Large mixed signal
intensity is seen with predominately solid mass (arrowheads)
extending into abdomen up to L3 level. Image shows superior and anterior
displacement of urinary bladder (small arrow) and dilated
fluid-filled vagina (large arrow) and uterus (double-headed
arrow). Moderate ascites are seen.
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Fig. 3B —29-weeks' gestation fetus with type III sacrococcygeal
teratoma. Coronal T2-weighted image shows small lungs (double-headed
arrow) and dilation of renal collecting systems (small arrows).
Renal cortex is heterogeneous with small cyst (arrowheads) present,
which is consistent with renal dysplasia.
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Fig. 3C —29-weeks' gestation fetus with type III sacrococcygeal
teratoma. Sagittal T1-weighted gradient-echo image shows displacement of
high-intensity meconium-filled colon (arrowheads) by pelvic and
abdominal mass (large arrows). Dilated fluid-filled vagina
(double-headed arrow) and superior displacement of
high-signal-intensity liver (small arrow) are seen.
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Results
In total, 22 fetuses with fetal sacrococcygeal teratoma were imaged. MR
images of diagnostic quality were obtained in all patients. Images from all MR
sequences were evaluated at the same time. The RARE sequence provided the best
overall image quality and produced the least amount of artifact resulting from
either motion or susceptibility effects. The image quality was decreased when
the mother was obese or in cases of polyhydramnios, which allows increased
fetal motion.
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Fig. 4A —22-weeks' gestation fetus with sacrococcygeal teratoma.
Oligohydramnios is seen. Image shows large, predominately solid, external mass
(arrowheads) with large intrapelvic and intraabdominal component.
Erosion of lower sacral spine (small arrow) and massive abdominal
ascites are shown. Thoracic cavity is small (double-headed arrow).
Severe skin and scalp edema (broad arrow) are consistent with
hydrops.
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Fig. 4B —22-weeks' gestation fetus with sacrococcygeal teratoma.
Sagittal T2-weighted image through maternal uterus shows marked heterogeneity
and enlargement of placenta (arrowheads) measuring 6 cm at greatest
width. Next to placenta is extrapelvic portion of sacrococcygeal teratoma
(double-headed arrow).
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On MRI, sacrococcygeal teratomas (n = 22) appeared entirely cystic
in five fetuses (macrocystic with a few septa in two, markedly septate in
three), microcystic in one, mixed cystic and solid in 12, and completely solid
in four. On the basis of prenatal MRI, the sacrococcygeal teratomas were
classified as type I in six patients (Fig.
1), type II in 12 (Fig.
2), type III in four (Figs.
3A,
3B, and
3C), and type IV in none. The
diagnostic features obtained at sonography agreed with the MRI findings in
three type I, eight type II, and three type III patients. Discrepancy between
prenatal MRI and sonography occurred in eight fetuses. Four fetuses with a
type I sacrococcygeal teratoma on sonography were assessed as type II on MRI,
three fetuses diagnosed with type II on sonography were type I sacrococcygeal
teratomas on MRI, and one fetus diagnosed with type II on sonography was a
type III sacrococcygeal teratoma on MRI.
The correct cephalic extent of the sacrococcygeal teratoma on
intraoperative findings or on autopsy correlated positively in all patients
with MRI. Intrapelvic mass effect—evident by displacement of the
bladder, hydronephrosis, large tortuous ureters, and urinary ascites—
was seen at MRI in nine of the 22 fetuses (41%), but this finding was seen in
only three of these nine patients by sonography. Dysplastic changes of the
kidneys were observed at MRI in five patients (unilateral, n = 2;
bilateral, n = 3), but in only two at sonography, which might be
related to the severe oligohydramnios seen in three of these five patients
(Figs. 4A and
4B). Similarly, on MRI it was
possible to estimate tumor compression of adjacent pelvic structures, which
was impossible on sonography. Anterior displacement of the colon was shown on
MRI in 11 (50%) fetuses. In three (two type with III and one with type II
sacrococcygeal teratoma) of these 11 patients, the colon was significantly
displaced against the anterior abdominal wall (Figs.
5A and
5B). A hip dislocation was
visible at MRI in four of 22 (18.2%) fetuses (two with type II and two with
type III sacrococcygeal teratoma) and diagnosed on sonography in only two. In
two fetuses, one with a sacrococcygeal teratoma type II and the other with
type III, the tumor extended into the spinal canal up to L3 and L1,
respectively. The extension into the spinal canal was not visible on
sonography in either case. One fetus with a mixed cystic and solid
sacrococcygeal teratoma showed a large intraabdominal cystic mass, discrete
from the tumor, between the tumor and the bladder. MRI showed the uterus
connected to this cystic lesion indicating an obstructed vagina. Sonography
was not able to determine the origin of the cystic mass.
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Fig. 5A —20-weeks' gestation fetus with sacrococcygeal teratoma type
II. Sagittal T2-weighted image shows mixed solid and cystic mass
(arrowheads) arising from coccyx. Intrapelvic extension (small
arrow) with anterior displacement of low-signal-intensity meconium-filled
colon (double-headed arrow) is seen.
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Fig. 5B —20-weeks' gestation fetus with sacrococcygeal teratoma type
II. Sagittal T2-weighted image shows external mass (arrowheads).
Dysplastic changes in renal cortex with multiple peripheral cortical cysts
(double-headed arrow) are evident. No significant dilation of this
renal collecting system is seen.
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Three patients elected to terminate the pregnancy. Fetal demise occurred in
four patients, three caused by cardiac failure and hydrops (placentomegaly,
effusions, ascites, and edema) and one caused by in utero tumor rupture. Three
fetuses in this series fulfilled our criteria (type I or II, high-output
physiology, and early hydrops) to be considered for fetal surgical
intervention and underwent fetal surgery (at 21-, 24-, and 26-weeks'
gestational ages), with two survivors
[20]. Four fetuses with mainly
cystic masses underwent sonography-guided in utero aspiration of the cysts.
Indications for cyst aspiration were maternal discomfort, preterm labor, and
prevention of tumor rupture at delivery. Four deaths were caused by tumor
rupture; in these cases, the neonates were premature, with a mean gestational
age of 29 weeks (range, 26-32.3 weeks). Two tumors ruptured during preterm
labor and two intraoperatively. The mean gestational age at delivery of the
survivors (excluding open fetal surgery patients, n = 8) was 36 weeks
(range, 33-38.5 weeks). All surviving fetuses were born by cesarean delivery
and underwent standard postnatal resection on day of life 1 or 2 without
further imaging studies. Pathologic examination performed for 11 of the
fetuses followed by our institution revealed mature (n = 4), immature
(n = 6), and mixed immature and mature (n = 1)
teratomas.
Discussion
Ultrafast MRI using sequences that acquire an image in less than 0.4
seconds allows fetal imaging without the necessity for fetal sedation or
paralysis [11]. To date,
several small case series have shown that prenatal MRI is useful in the
assessment of sacrococcygeal teratoma
[11,
17,
18]. However, the question
remains whether MRI is equivalent, superior, or complementary to sonography
for prenatal assessment of sacrococcygeal teratoma. To be generally accepted,
a newly applied diagnostic device must fulfill a number of requirements.
First, it must be safe and not expose the patient to unnecessary risks.
Second, it must be able to diagnose the underlying problem. Third, it should
provide additional useful information that is not provided by a currently
established method. Finally, in the current fiscal environment, the new
diagnostic procedure should be cost-effective. Our results suggest that MRI
fulfills these criteria for diagnostic evaluation of fetal sacrococcygeal
teratoma. Multiple experimental and clinical studies support the safety of MRI
for fetal imaging [16,
21-23].
Although the potential exists for teratogenic effect, we limit MRI to fetuses
at more than 18 weeks' gestation and have seen no ill effects attributable to
MRI. Our results clearly show that MRI is superior to sonography in assessing
the intrapelvic and intraspinal extent of tumor and in discerning the presence
and physiologic effects of compression of pelvic organs by the tumor. These
advantages allow more accurate prognostic counseling for patients presenting
with sacrococcygeal teratoma and improve pre- and perinatal management by
providing accurate data for decisions regarding fetal surgery, tumor
decompression, and timing of delivery.
Optimal management of fetal sacrococcygeal teratoma requires accurate
imaging of the precise intrapelvic and intraabdominal extent of tumor, the
content of the tumor, and the physiologic effects of tumor compression on the
pelvic organs or bone structure. MRI proved superior to sonography in all of
these requirements. Our results show that sonography does not always precisely
assess the intrapelvic extension of the tumor. The advantage of MRI is
primarily related to the absence of acoustic shadowing by the fetal pelvic
bones that interferes with sonography visualization. In our series, the
cephalad extension of the tumor was misdiagnosed using sonography in eight of
22 (36%) fetuses. Sonography underestimated the pelvic and intraabdominal
extent of tumors in five fetuses (type I rather than type II in four fetuses,
type II rather than type III in one) and overestimated the extent of tumor in
three fetuses (type II rather than type I).
MRI also enhanced the assessment of the content of sacrococcygeal teratoma.
Fetal sacrococcygeal teratoma may be cystic, solid, or mixed in sonographic
appearance and may contain characteristic echogenic patterns secondary to
areas of tumor necrosis, cystic degeneration, internal hemorrhage, and
calcification [8]. The
prognosis of prenatally detected sacrococcygeal teratoma seems to be related
not only to the size of the mass but also to its content. Fetuses with
predominantly solid and highly vascularized masses have a poorer prognosis
than fetuses with tumors that are mainly cystic and avascular in appearance.
The solid, vascularized masses require closer surveillance for the evolution
of high-output physiology
[24]. Sonography seems to be
sufficient for evaluating mainly cystic and extrapelvic sacral masses;
however, when the tumor appears to be echogenic, it is more difficult for
sonography to characterize the sacrococcygeal teratoma content. Echogenicity
can result from a solid component or hemorrhage. Hemorrhage can be seen on MRI
with T1-weighted or echo-planar images. This is particularly important in
fetuses with evolving hydrops because high-output physiology may result from
fetal anemia rather than from tumor-related vascular steal. In conjunction
with Doppler sonography, which remains the most accurate way to measure tumor
vascularity and physiologic effect on the cardiovascular stability of the
fetus, the presence of hemorrhage on MRI in the tumor should prompt an
evaluation of fetal anemia. Fetuses with large echogenic tumors on MRI need
frequent monitoring using sonography and echocardiography for evolution of
high cardiac output physiology to determine the need for intervention
[20].
Tumor involvement or compression of adjacent organs is an important
contributor to the morbidity of sacrococcygeal teratoma, and accurate prenatal
assessment is important for the timing of intervention and comprehensive
prenatal counseling. Urologic complications are the most common cause of
morbidity from sacrococcygeal teratoma, occurring in at least 41% of our
patients. Tumor compression of the bladder outlet caused urinary retention
followed by secondary renal deterioration, oligohydramnios, and pulmonary
hypoplasia in one fetus. Other published series have described severe urologic
problems with prenatally detected sacrococcygeal teratoma
[25-27].
The highest incidence of urologic complications in our series (67%) was seen
in patients with type III tumors. Furthermore, damage to the innervation of
the lower urinary tract in sacrococcygeal teratoma may be caused by
compression or infiltration of sacral nerves by the tumor; intraspinal
extension of the tumor; or trauma to the pelvic, splanchnic, or hypogastric
nerves during tumor resection
[28]. However, long-term
urologic sequelae of our surviving patients with sacrococcygeal teratoma have
not been well defined because most of the children are currently younger than
6 years. Renal failure may not develop acutely after long-term obstruction
even in the presence of renal dysplasia. Renal failure may not occur until the
end of the first decade of life. Accurate diagnosis and classification of
sacrococcygeal teratoma during pregnancy and long-term follow-up studies are
essential to evaluate the clinical impact of urologic complications seen in
prenatally diagnosed sacrococcygeal teratoma.
Surgeons at our institution found that MR images helped them mentally
visualize the content and extent of the sacrococcygeal teratoma before
delivery. In most cases, neonatal surgery is required soon after cesarean
delivery, and the anatomic details of tumor extent and involvement of adjacent
structures may affect the surgical approach. No postnatal tumor imaging was
done before surgery. In two fetuses, extension into the spinal canal was
visible only on MRI. Patients with significant intrapelvic extension of the
tumor may need a combined abdominoperineal approach to control the blood
supply and achieve complete surgical resection. The colon is well visualized
and distinguished from an intraabdominal sacrococcygeal teratoma because the
meconium has high signal intensity on T1-weighted images, providing valuable
information about atypical colon deviation or involvement before surgery. MRI
provides an image of the fetus that is easier to understand than a sonography
image for physicians and patients not familiar with sonography performance and
interpretation. This may help avoid resection-related complications such as
urologic functional abnormalities and fecal incontinence
[4].
Our results show that ultrafast fetal MRI is a powerful addition to the
prenatal evaluation of fetuses with sacrococcygeal teratoma. Based on our
experience using prenatal MRI for evaluation of fetal sacrococcygeal teratoma,
we recommend that all fetuses with appearance of sacrococcygeal teratoma on
sonography undergo MRI evaluation to assess exact tumor size, content, and
intraabdominal extent to optimize pre-, peri-, and postnatal management.
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Abstract
Introduction
