MR Imaging Differentiation of Soft

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MR Imaging Differentiation of SoftTissue Hemangiomas from
Malignant Soft-Tissue Masses
Eu-Leong H. J. Teo 1,2
Peter J. Strouse 1
Ramiro J. Hernandez 1
OBJECTIVE. The purpose of this study was to determine whether MR imaging features
can reliably distinguish hemangiomas from malignant soft-tissue masses.
MATERIALS AND METHODS. We retrospectively reviewed MR imaging studies of 22
patients with soft-tissue hemangiomas and 22 patients with malignant soft-tissue masses. Images
were reviewed and agreement reached by a consensus interpretation of two observers and by an independent observer. Masses were evaluated for signal intensity on T1- and T2-weighted images,
for enhancement with gadolinium administration, and for morphology (lobulation, septation, central low-intensity dots). Lesion T2 signal and lesion enhancement with gadolinium administration
were also objectively measured using regions of interest and comparison with skeletal muscle.
RESULTS. Signal intensity on T1-weighted imaging of hemangiomas and malignant soft-tissue masses was similar. Subjective analysis showed greater T2 signal and gadolinium enhancement in hemangiomas; however, the differences were not statistically significant on objective
analysis. Lobulation, septation, and central low-signal-intensity dots were all more common in
hemangiomas, with statistical significance achieved; the combination of all three findings was
specific for hemangioma.
CONCLUSION. Although no single MR imaging feature was diagnostic in this study,
analysis of lesion morphology, signal intensity, and enhancement with gadolinium allowed
MR imaging differentiation of hemangiomas from malignant soft-tissue masses.
H
Received July 20, 1999; accepted after revision
November 3, 1999.
Presented at the annual meeting of the American
Roentgen Ray Society, Boston, May 1997.
1
Section of Pediatric Radiology, Department of Radiology,
C. S. Mott Children’s Hospital, University of Michigan
Health Centers, Ann Arbor, MI 48109-0252. Address
correspondence to R. J. Hernandez.
2
Present address: 26 Leedon Rd., Singapore 1026.
AJR 2000;174:1623–1628
0361–803X/00/1746–1623
© American Roentgen Ray Society
AJR:174, June 2000
emangiomas are common neoplasms that account for 7% of all
benign soft-tissue tumors [1]. Although the biologic classification of vascular
anomalies proposed by Mulliken and Glowacki
[2] separates hemangioma of infancy from vascular malformations, the term “hemangioma” is
used in this article to generically encompass hemangiomas and vascular malformations.
Most patients with deep-seated hemangiomas
present with either pain or intermittent swelling.
Patients occasionally describe a poorly delineated mass that becomes larger or smaller from
time to time. Deep-seated hemangiomas cannot
be distinguished from malignant soft-tissue tumors without imaging studies. When imaging
can distinguish hemangiomas from malignant
soft-tissue tumors, patient management is affected regarding the need for further imaging or
biopsy and the choice of therapy.
Other researchers have described the MR
imaging features of hemangiomas [1, 3–5].
Some studies have indicated that hemangiomas may be correctly diagnosed and distin-
guished from malignant soft-tissue masses by
their characteristic MR appearances [6–8].
Our objective in this study was to compare
the MR imaging features of hemangiomas
with those of malignant soft-tissue masses
and to determine the combination of features
that would allow hemangiomas to be distinguished from malignant soft-tissue masses.
Materials and Methods
The MR images of 22 patients with peripheral
hemangiomas and 22 patients with primary malignant soft-tissue masses were retrospectively reviewed. The patients were consecutively imaged at
our institution between 1992 and 1997 for hemangiomas and between 1995 and 1997 for the malignant soft-tissue masses. All patients were imaged
before biopsy or surgery, when performed.
The age range of the patients with hemangiomas
was 2–43 years (median, 12 years) and with malignant soft-tissue masses was 3 months to 87 years
(median, 53 years). Of the 22 hemangiomas, the diagnosis (three arterial venous malformations, two
venous malformations, one benign vascular mal-
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Teo et al.
formation, one cavernous hemangioma, three hemangiomas) was made histologically in 10
patients, on angiography in six, and by the characteristic clinical findings and follow-up in the remaining six patients. Malignant soft-tissue masses
were confirmed histologically in all 22 patients.
The soft-tissue masses were seven malignant fibrous histiocytomas, five rhabdomyosarcomas, two
neurofibrosarcomas, two primitive neuroectodermal tumors, and six other soft-tissue sarcomas.
All patients were imaged using a Signa 1.5-T
scanner (General Electric Medical Systems, Milwaukee, WI). T1- and T2-weighted images were acquired in all patients. Eleven hemangiomas and 21
malignant soft-tissue masses were imaged after IV
gadolinium administration (gadopentetate dimeglumine, 0.1 mmol/kg) using T1-weighted images with
fat saturation. Gadolinium-enhanced images were
obtained with a short delay after administration.
The images were interpreted without knowledge
of the final diagnosis of the soft-tissue mass or patient age. Two radiologists reviewed the images and
arrived at a consensus interpretation of the imaging
features. A third radiologist reviewed the images independently after being educated with regard to the
imaging definitions. The purpose of the third reader
was to provide a reliability measure for the imaging
criteria used. The masses were evaluated for the signal intensity of the lesions on unenhanced T1weighted images, gadolinium-enhanced T1-weighted
images, and T2-weighted images and for the morphologic features of the lesions: lobulation, septation,
and the presence of central low-signal-intensity dots
on T2-weighted images. Signal intensity was characterized as isointense or mildly, moderately, or
TABLE 1
markedly hyperintense compared with the signal intensity of skeletal muscle. A lesion was considered
lobulated if it showed internal septations resulting
in a grapelike configuration (Figs. 1 and 2). It was
considered septate if internal divisions or septa subdivided it into several smaller compartments (Fig.
3). The central low-signal-intensity dot sign on T2weighted images was deemed to be present if at
least three or more punctate central low-signal-intensity dots were present in the center of the lobulation (Fig. 2).
To obtain objective evaluation of the signal intensities of the lesions, measurements of regions
of interest of representative portions of the lesions
were compared with similar sized regions of interest in adjacent skeletal muscle. A ratio between the
two signal intensities was calculated for each
lesion seen on both gadolinium-enhanced T1weighted images and unenhanced T2-weighted
images. The T2 relaxation time of the lesions was
calculated for 18 hemangiomas and eight malignant soft-tissue masses in which dual-echo imaging was performed. T2 was calculated using the
formula: T2 = (TE2 – TE1) / (Ln [ROI1 / ROI2]),
where TE1 = time to first echo (msec), TE2 = time
to second echo (msec), Ln = natural logarithm,
ROI1 = signal intensity of region of interest on first
echo, and ROI2 = signal of intensity of region of
interest on second echo.
Statistical analysis was performed using the
chi-square test for categoric data and the independent t test for continuous data. The agreement between the consensus and the independent readings
was assessed using the kappa statistic. Statistical
significance was set at the 0.05 level.
Frequency of Lobulations, Septations, and Central Low-Signal-Intensity Dots
in Hemangiomas and Malignant Soft-Tissue Masses on T2-Weighted Imaging
Lobulation
Central Low-SignalIntensity Dots
Septation
Feature Imaged
Hemangiomas (n = 22)
Malignant soft-tissue masses (n = 22)
A
B
A
B
A
B
21
5
19
8
22
15
19
2
21
0
18
2
Note.—A = consensus interpretation by two radiologists, B = interpretation by one radiologist.
TABLE 2
Frequency of Combined
Lobulations, Septations, and
Central Low-Signal-Intensity
Dots in Hemangiomas and
Malignant Soft-Tissue Masses
on T2-Weighted Imaging
Fig. 1.—Diagram shows septations and lobulations. In
a septate mass, septa do not form lobulations.
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Characteristics on T1-Weighted Images
T1-weighted images showed no reliable distinguishing features. Both hemangiomas and
soft-tissue tumors were low in signal intensity.
Characteristics on T2-Weighted Images
The frequency of lobulation, septation, and
central low-intensity dots on T2-weighted images was much higher for hemangiomas than
for malignant soft-tissue tumors (Table 1).
This difference was statistically significant for
the consensus and independent readings.
Masses with all three imaging characteristics
(lobulations, septations, and central low-intensity dots) present were exclusively hemangiomas, independent of whether the consensus or
independent readings were used (Table 2). Hemangiomas frequently had a lobulated appearance and central low-intensity dot. On the
other hand, malignant soft-tissue tumors occasionally had septations and rarely had a central
low-intensity dot.
The T2 signal intensities of hemangiomas
were generally higher than those of malignant
soft-tissue masses (Table 3). Although subjective, this difference was found to be statistically significant for both the consensus and
independent readings. Although the quantitative analysis revealed higher values of signal
intensity ratios for hemangiomas than for malignant soft-tissue masses (Fig. 4), no statistical significance was observed.
Characteristics on Gadolinium-Enhanced
T1-Weighted Images
In general, hemangiomas were judged to
enhance markedly compared with malignant
soft-tissue tumors (Table 4). This difference
was statistically significant for both the consensus and independent readings. Although
the median of the signal-intensity ratios for
hemangiomas was higher than the median
for malignant soft-tissue masses (Fig. 5), the
difference was not statistically significant.
Calculated T2 Relaxation Times
Present
Absent
A
B
A
B
In general, hemangiomas had a higher T2
relaxation time than malignant soft-tissue
masses (Fig. 6); however, the difference in
calculated T2 relaxation times between hemangiomas and malignant soft-tissue masses
was not statistically significant.
20
0
16
0
2
22
6
22
Consensus Versus Independent Readings
Feature Imaged
Hemangiomas (n = 22)
MSTM (n = 22)
Results
Note.—A = consensus interpretation by two radiologists,
B = interpretation by one radiologist, MSTM = malignant softtissue masses.
Substantial agreement occurred between the
two readings for the assessment of lobulations
and central-low intensity dots (κ = 0.62–0.68),
AJR:174, June 2000
MR Imaging of Soft-Tissue Hemangiomas
B
A
Fig. 2.—10-year-old boy with hemangioma of lower extremity.
A, Axial T1-weighted MR image (TR/TE, 500/16) shows low signal intensity of tumor (arrows) with interspersed areas of high signal intensity representing fat.
B, Axial T2-weighted MR image (4000/85) shows lobulated high-signal-intensity
lesion. Note several central low-signal-intensity dots (arrows).
C, Gadolinium-enhanced T1-weighted MR image (500/16) shows marked enhancement of lesion. Central low-intensity dots seen on B are not seen after
contrast administration, suggesting vascular nature.
C
TABLE 3
Subjective Evaluation of T2 Signal Intensity of Hemangiomas and Malignant
Soft-Tissue Masses Compared with Skeletal Muscle
Isointense
Mild
Moderate
Marked
Feature Imaged
Hemangiomas (n = 22)
MSTM (n = 22)
A
B
A
B
A
B
A
B
0
1
0
1
1
8
0
6
0
8
0
6
21
5
22
9
Note.—A = consensus interpretation by two radiologists, B = interpretation by one radiologist, MSTM = malignant soft-tissue
masses.
moderate agreement for the signal characteristic on T2-weighted images and the degree of
enhancement after gadolinium (κ = 0.5–0.53),
and fair agreement for the assessment of septation (κ = 0.3).
AJR:174, June 2000
Discusson
This study shows that hemangiomas have
characteristic MR imaging features that enable
their differentiation from malignant soft-tissue
masses without the need for biopsy. Specifi-
cally, these features are the lobulated and septate
appearance of hemangiomas compared with
malignant soft-tissue masses; the central low-intensity dot sign on T2-weighted imaging characteristically seen in hemangiomas; marked
enhancement of hemangiomas after gadolinium
administration on T1-weighted imaging; and
the high T2 signal of hemangiomas compared
with that of malignant soft-tissue masses. It is
the summation of all these features, rather than
any one particular feature taken in isolation,
that will help the radiologist make a diagnosis
of hemangioma.
Although hemangiomas and vascular malformations constitute a continuum of pathologic
abnormality, our study suggests that these le-
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Teo et al.
distinction; however, it highlights the importance
of distinguishing benign from malignant soft-tissue masses. In this paper, we have therefore used
the generic term “hemangioma” to encompass
sions may as a group manifest MR imaging
characteristics that distinguish them from malignant soft-tissue masses. Admittedly, the grouping of a continuum of lesions blurs their
TABLE 4
Evaluation of Degree of Gadolinium Enhancement of Hemangiomas and
Malignant Soft-Tissue Masses
No Enhancement
Mild
Moderate
Marked
Feature Imaged
Hemangiomas (n = 11)
MSTM (n = 21)
A
B
A
B
A
B
A
B
0
1
0
0
4
11
1
6
2
8
2
9
5
1
8
6
Note.—A = consensus interpretation by two radiologists, B = interpretation by one radiologist, MSTM = malignant soft-tissue
masses.
all hemangiomatous lesions and vascular malformations, although pathologic and imaging
distinctions exist [2, 9]. Histologically, hemangiomas are vascular lesions containing nonvascular elements such as fat, fibrous and myxoid
tissue, smooth muscle, thrombus, and even bone
[10]. The MR imaging appearance of deep peripheral hemangiomas has been well described
in the literature [1, 3–5, 11, 12].
Characteristics on T2-Weighted Imaging
On T2-weighted images, hemangiomas have
been described as having a multilobulated
high-signal-intensity configuration interspersed
B
A
Fig. 3.—7-year-old girl with malignant sarcoma of lower extremity.
A, Axial T2-weighted MR image (TR/TE, 4500/90) shows high-signal-intensity mass posterior to femur. Note septations within mass, giving mass slightly lobulated appearance. Also note low-signal-intensity dots within mass (arrows); however, dots are not centrally located in a lobulation.
B, T1-weighted image (500/8) shows marked enhancement. Low-signal-intensity dots (arrow ) in mass remain visible.
Fig. 4.—Box plot shows signal-intensity ratios between tumor and muscle
on T2-weighted MR imaging. Note
that signal-intensity ratios are higher
for hemangiomas than for malignant
tumors. Upper margin of each box
represents 75th percentile; lower
margin represents 25th percentile.
Line in middle of box represents median. Stars indicate outside values.
4
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5
Fig. 5.—Box plot shows signal intensity ratio between tumor and
muscle on T1-weighted imaging after gadolinium administration. Note
that enhancement with contrast
material was higher for hemangiomas than for malignant soft-tissue
tumors. Upper margin of box represents 75th percentile; lower margin
represents 25th percentile. Line in
middle of box represents median.
Star indicates outside values.
AJR:174, June 2000
MR Imaging of Soft-Tissue Hemangiomas
Fig. 6.—Box plot shows calculated T2weighted MR imaging of hemangiomas and
malignant soft-tissue tumors. Note higher
values for hemangiomas. Upper margin of
box represents 75th percentile; lower margin
represents 25th percentile. Line in middle of
box represents median. Circle indicates faroutside value.
with linear and lacelike areas of low or intermediate signal intensity [1, 3, 4, 12]. This morphologic appearance is supported by our study.
These findings were also shown by Cohen et al.
[13], who suggested that the distinctive septate–lobulated appearance on T2-weighted imaging correlated with fibrous and fatty septa
(low signal) between endothelial-lined vascular
channels (high signal) identified on histologic
examination. Our study suggests that the T2
signal intensity of hemangiomas is greater than
that of malignant soft-tissue masses, although
the quantitative assessment was not shown to
be statistically significant. The lack of statistical significance was probably caused by the
small sample in which this quantitative analysis
was performed. The T2 signal intensity of lesions is a reflection of their T2 relaxation times.
Hemangiomas have high T2 values, which may
reflect pooling of the blood within cavernous
spaces and slow flow within dilated venous
channels [5]. Buetow et al. [3] suggested that
the high T2 signal intensity of hemangiomas
appeared to be related to increased free water in
stagnant blood pooled in the larger vessels of
lesions. The calculated T2 was not significantly
different between hemangiomas and malignant soft-tissue masses in our study. However,
the small numbers of malignant soft-tissue
masses for which the T2 value could be calculated may have contributed to the lack of statistical significance.
The central low-intensity dot sign on T2weighted imaging in hemangiomas has been
previously described [1]. Our study has shown
that this sign is highly specific for hemangiomas compared with malignant soft-tissue
masses. These rounded foci of low signal intensity seen in hemangiomas may represent fibrofatty septa seen in cross section, or
hyalinized or thrombosed vascular channels
AJR:174, June 2000
[4]. Hawnaur et al. [11] have also suggested
that smooth muscle components, fast flow
within blood vessels, calcification, or ossification may give rise to this appearance. The central low-intensity dots are not likely to
represent phleboliths because they were not
recognizable on the T1-weighted images or
on conventional radiographs. Fast flow in
blood vessels is a likely cause in some cases
because the central low-intensity dots disappear after gadolinium administration (Fig.
2C). This central low-intensity dot has also
been described in benign neurofibromas,
where it produces a so-called targetlike appearance [14, 15]. The pattern of enhancement is helpful in distinguishing between
neurofibromas and hemangiomas. Because
the central low-intensity dot in benign neurofibromas is caused by dense collagen, it is
not likely to exhibit enhancement with gadolinium as hemangiomas do [15].
Characteristics on T1-Weighted
Gadolinium-Enhanced Images
Qualitative assessment revealed that hemangiomas showed a greater degree of enhancement
with gadolinium than did malignant soft-tissue
masses. Quantitative assessment of enhancement with gadolinium showed that the median
of the region-of-interest ratios of hemangiomas
was greater than that of malignant soft-tissue
masses; however, the difference was not statistically significant. The small sample of hemangiomas in which gadolinium had been given may
have contributed to the lack of statistical significance. Intense enhancement, therefore, is supportive of the diagnosis of hemangioma but
should be used in corroboration of other findings
to reach the diagnosis.
We did not specifically analyze whether
the presence of fat or its distribution in the
lesion was a feature distinguishing hemangiomas from malignant soft-tissue masses. Fatcontaining malignant soft-tissue masses are
rare in children. Although intercalated fat is a
feature of hemangiomas, other fat-containing
soft-tissue masses, most notably lipoblastoma, do occur in children [16, 17].
A possible limitation of this study is the
small number of patients in both lesion groups
in whom the quantitative parameters could be
evaluated. This may have contributed to the
lack of statistical significance in the differences in the T2 signal intensities, T2 relaxation
times, and lesion enhancement with gadolinium in the objective parts of the study.
A second limitation was the difference in
the age ranges of the two patient populations.
The group of patients with hemangiomas had
an age range that was substantially lower than
the age range of patients with malignant softtissue masses. The difference in age in our
study between the two patient populations
was necessitated by the relatively small number of malignant soft-tissue masses imaged
with MR in pediatric patients. The difference
in age range is not thought to be critical because the morphology of malignant soft-tissue masses on MR imaging is unlikely to be
affected by the age of patients. The age of the
patient in itself should not be overlooked as
valuable information in helping to distinguish
hemangiomas from malignant soft-tissue
masses. Other clinical factors, such as chronicity of the mass and a rapid increase in its
size, are also helpful.
A third limitation of this study is the subjective assessment of imaging features such as
septation, lobulation, and the degree of enhancement after gadolinium administration.
Different observers may develop different
thresholds, which is reflected by some degree
of discrepancy in the assessment of septations
and lesion enhancement between the consensus reading and the independent reader in our
study. However, despite this variability and regardless of whether the consensus or independent readings are used, the combination of
imaging findings (lobulation, septation, and
central low-intensity dot) has predictive value.
Last, this investigation is limited by the
relatively small number of patients studied. It
was not possible to include all types of malignant soft-tissue tumors in this analysis.
Boon et al. [18] reported two cases of congenital fibrosarcoma mimicking congenital
hemangioma. No case of this tumor was included in our study. Although it is possible
that application of our criteria allowed the
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Teo et al.
correct diagnosis, further analysis of a larger
number of patients with a wider spectrum of
malignant soft-tissue masses is warranted.
In summary, this study suggests that hemangiomas can be distinguished from malignant
soft-tissue masses on MR imaging by using a
combination of morphologic features, the degree of enhancement after the administration of
gadolinium, and the T2 signal intensity, potentially obviating biopsy in many cases.
References
1. Suh JS, Hwang G, Hahn SB. Soft-tissue hemangiomas: MR manifestations in 23 patients. Skeletal
Radiol 1994;23:621–625
2. Mulliken JB, Glowacki J. Hemangiomas and vascular malformations in infants and children: a
classification based on endothelial characteristics.
Plast Reconstr Surg 1982;69:412–420
3. Buetow DC, Kransdorf MJ, Moser RP Jr, Jelink
JS, Berrey BH. Radiological appearance of intramuscular hemangioma with emphasis on MR imaging. AJR 1990;154:563–567
4. Kaplan PA, Williams SM. Mucocutaneous and
peripheral soft-tissue hemangiomas: MR imaging. Radiology 1987;163:163–166
1628
5. Jenner G, Soderlund V, Bauer HFC, Brosjo O.
MR imaging of skeletal muscle hemangiomas.
Acta Radiol 1996;37:140–144
6. Berquist TH, Ehman RL, King BF, Hodgman CG,
Ilstrup DM. Value of MR imaging in differentiating benign from malignant soft-tissue masses:
study of 95 lesions. AJR 1990;155:1251–1255
7. Crim JR, Seeger LL, Yao L, Chadnani V, Eckhardt
JJ. Diagnosis of soft-tissue masses with MR imaging: can benign masses be differentiated from malignant ones? Radiology 1992;185:581–586
8. Moulton JS, Blebea JS, Dunco DM, Braley SE,
Bisset GS III, Emery KH. MR imaging of softtissue masses: diagnostic efficacy and value of
distinguishing between benign and malignant lesions. AJR 1995;164:1191–1199
9. Meyer JS, Hoffer FA, Barnes PD, Mulliken JB. Biological classification of soft-tissue vascular anomalies: MR correlation. AJR 1991;157:559–564
10. Allen PW, Enzinger FM. Hemangioma of the
skeletal muscle: an analysis of 89 cases. Cancer
1972;29:8–22
11. Hawnaur JM, Whitehouse RW, Jenkins JPR, Isherwood I. Musculoskeletal haemangiomas: comparison of MRI with CT. Skeletal Radiol 1990;19:
251–258
12. Greenspan A, McGahan JP, Vogelsang P, Szabo
RM. Imaging strategies in the evaluation of soft-
13.
14.
15.
16.
17.
18.
tissue hemangiomas of the extremities: correlation
of the findings of plain radiography, angiography,
CT, MRI and ultrasonography in 12 histologically
proven cases. Skeletal Radiol 1992; 21:11–18
Cohen EK, Kressel HY, Perosio T, et al. MR imaging of soft-tissue hemangiomas: correlation with
pathologic findings. AJR 1988;150:1079–1081
Suh JS, Abenoza P, Galloway HR, Everson LI,
Griffiths HJ. Peripheral [extracranial] nerve tumors: correlation of MR imaging and histologic
findings. Radiology 1992;183:341–346
Bhargava R, Parha DM, Lasater OE, Chari RS,
Chen G, Fletcher BS. MR imaging differentiation
of benign and malignant peripheral nerve sheath
tumors: use of the target sign. Pediatr Radiol
1997;27:124–129
Murphey MD, Fairbairn KJ, Parman LM, Baxter
KG, Parsa MB, Smith WS. Musculoskeletal angiomatous lesions: radiologic-pathologic correlation. RadioGraphics 1995;15:893–917
Reiseter T, Nordshus T, Borthne A, Roald B,
Naess P, Schistad O. Lipoblastoma: MRI appearances of rare paediatric soft tissue tumour. Pediatr Radiol 1999;29:542–545
Boon LM, Fishman SJ, Lund DP, Mulliken JB.
Congenital fibrosarcoma masquerading as congenital hemangioma: report of two cases. J Pediatr Surg 1995;30:1378–1381
AJR:174, June 2000
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