Title Page
© 2016 The Authors. Published by the British Institute of Radiology
Usefulness of Diffusion-Weighted MR Imaging for Differentiating between Benign and
FS
Malignant Superficial Soft Tissue Tumors and Tumor-like Lesions
O
Ji Young Jeon, M.D., Hye Won Chung, M.D., Min Hee Lee, M.D., Sang Hoon Lee, M.D., Myung Jin
O
Shin, M.D.
Department of Radiology and Research Institute of Radiology, University of Ulsan College of
P
R
Medicine, Asan Medical Center
D
Ji Young Jeon, M.D.: First author
C T
E
E-mail: [email protected]
Min Hee Lee, M.D. : [email protected]
R R E
Sang Hoon Lee, M.D.: [email protected]
U
N
C
O
Myung Jin Shin, M.D. : [email protected]
Address to Correspondence: Hye Won Chung, M.D.
B
JR
Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, 88, Olympic-Ro 43-Gil, Songpa-Gu Seoul 138-736, Korea e-mail: [email protected]
Objectives: To evaluate the usefulness of adding DW imaging with ADC mapping to conventional 3.0-T MR imaging to differentiate between benign and malignant superficial soft tissue masses (SSTMs). Methods: The institutional review board approved this study and informed consent was waived. The authors
FS
retrospectively analyzed conventional MR images including DW images (b-values: 0, 400, 800sec/mm2) in 60 histologically proven SSTMs (35 benign; 25 malignant) excluding lipomas. Two radiologists independently evaluated the conventional MRI alone and again with the additional DWI for evaluation of malignant masses.
B
O
The mean ADC values measured within an entire mass and the contrast enhancing solid portion were used for
O
quantitative analysis. Diagnostic performances were compared using ROC analysis.
Results: For an inexperienced reader, using only conventional MRI, sensitivity, specificity and accuracy were
R
84%, 80% and 81.6%, respectively. When combining conventional MRI and DWI, the sensitivity, specificity
P
and accuracy were 96%, 85.7% and 90%, respectively. Additional DWI influenced the improvement of the rate of correct diagnosis by 8.3% (5/60). For an experienced reader, additional DWI revealed the same accuracy of
D
86.7% without added value on the correct diagnosis. The group mean ADCs of malignant SSTMs was significantly lower than that of benign SSTM (P< .001). The best diagnostic performance with respect to
E
differentiation of SSTMs could be obtained when conventional MR imaging was assessed in combination with
C T
DW imaging.
Conclusions: Adding qualitative and quantitative DWI to conventional MR imaging can improve the diagnostic performance for differentiation between benign and malignant SSTMs.
R R E
.
Advances in knowledge: Because the imaging characteristics of many malignant superficial soft tissue lesions overlap with those of benign ones, inadequate surgical resection due to misinterpretation of MR imaging often occurs. Adding diffusion-weighted imaging to conventional MR imaging yields greater diagnostic performances
O
(area under the receiver operating characteristic curve [AUC], 0.83–0.99) than does use of conventional MR
N
C
imaging alone (AUC, 0.71–0.93) in the evaluation of malignant superficial masses by inexperienced readers.
U
Key Words:
Superficial soft-tissue masses, Magnetic resonance imaging, diffusion, ADC, Malignant superficial soft-tissue tumors
JR
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
Abbreviations: ADC = apparent diffusion coefficient DW = diffusion-weighted
ROC = receiver operating characteristic
FS
ROI = region of interest
Superficial soft-tissue masses are a common reason for visiting the outpatient clinics. As the availability of radiologic imaging has expanded, the chance of encountering any superficial soft tissue masses (SSTMs) for
O
radiologists has also been increased. In the case of some SSTMs, such as lipomas, a definitive diagnosis is not
B
O
difficult using conventional MR imaging only because of their characteristic fatty component. However, in much clinical practice, the differentiation between benign and malignant SSTMs using only conventional MR problematic as many of their imaging features are nonspecific and some overlap exists between the
R
imaging is
P
malignant and benign groups 1. Diffusion-weighted imaging (DWI) measures the random motion of water protons in tissue. The random Brownian motion of water protons determines DWI signal intensity, and the quantitative assessment of water diffusion in tissues is expressed as the apparent diffusion coefficient (ADC)
assessing soft tissue tumors have been widely investigated
2,3
. Although the usefulness of DW imaging for
E
tissue from that attained using conventional MR techniques
D
values. Because of this, the diffusion-weighted (DW) procedure provides different tissue contrast about diseased 2,4-6
, there are not many publications that separately
C T
evaluating the usefulness of DW imaging for superficial soft tissue masses. The purpose of our study is to retrospectively determine specifically the value of adding DW imaging with ADC mapping to conventional 3.0-
R R E
T magnetic resonance imaging to differentiate between benign and malignant SSTMs.
Materials and Methods
O
Patient population
C
Our institutional review board approved this study, and waived the requirement for informed consent.
N
Since August 2013, MR imaging that included axial DW imaging at 3.0-T has been performed for soft tissue masses at our institution. From August 2013 to April 2015, all of the consecutive patients who underwent MR
U
imaging with DW imaging for evaluation of soft tissue masses localized to the trunk or the extremities, were retrospectively evaluated. Two hundred and thirty two patients were identified on the initial survey. One hundred and thirty-eight patients did not undergo histopathological confirmation and were thus excluded from
JR
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
our study.
The 94 patients remaining with superficially located lesions were further filtered for image quality,
previous excision/surgery and size as well as pathology indicating lipoma by a radiologist (J.Y.J.) with two years of experience in musculoskeletal radiology. SSTMs were defined as lesions located within the subcutaneous fat, and superficial to the superficial investing fascia, which separates the subcutaneous tissue layer from the underlying muscle on conventional MR imaging 1,7. Fourteen patients were excluded due to : image distortion of DW imaging (n= 6), previous treatment such as excision or excisional biopsy (n=5), and lesions less than 5mm in maximum diameter, as these were too small to further characterize on conventional MR imaging (n =3). Patients were also excluded who had lipomas (n =20) determined on pathologic confirmation. Finally, a total of
60 patients (mean age, 48.5 years; age range, 5–80 years; 30 men [mean age, 47.2 years; age range, 5–80 years] and 30 women [mean age, 49.8 years; age range, 14–71 years]) with SSTMs were included in our study. The
FS
detailed histopathologic diagnoses are listed in Table 1.
O
MR Imaging Protocols
All examinations were performed on a 3-T scanner (Achieva; Philips Medical Systems, Best, the Netherlands)
O
system. Depending on the localization of the tumor, dedicated surface coils were used. The conventional MR imaging protocols included axial T1-weighted turbo spin-echo (TSE) sequence, axial T2-weighted TSE
R
sequences with and without fat suppression, coronal or sagittal T1-weighted TSE sequence, and coronal or
P
sagittal T2-weighted TSE sequence with and without fat suppression. In all 60 patients, axial, coronal, and sagittal fat-suppressed contrast–enhanced T1-weighted sequences were also performed. Before the commencement of this diffusion MR study, a series of image quality tests were performed to adjust acquisition
D
parameters of diffusion and total scan time. A single-shot spin-echo echo-planar DW sequence was performed in
E
axial planes. A parallel imaging technique using sensitivity encoding, or SENSE, was combined with an acceleration factor of 1.5. The echo-planar imaging factor was 67, and sensitizing diffusion gradients were
C T
applied sequentially in the x, y, and z directions with b values of 0, 400, and 800 sec/mm 2 8. The ADC maps were automatically calculated using commercial software and were included in the sequences. The sequence
MR Imaging Analysis
R R E
parameters are presented in Table 2.
O
To assess the added value of DW imaging in the differentiation of malignant from nonmalignant superficial soft tissue lesions, the diagnostic performance of conventional MR imaging alone and additional DW imaging with
C
ADC mapping was compared. To evaluate conventional MR imaging alone, two musculoskeletal radiologists (H.W.C., J.Y.J.; 19-years and 2-years of clinical experience in musculoskeletal MR imaging, respectively)
N
independently reviewed the conventional MR images of 60 patients, both being unaware of the previous
U
imaging reports and the patients’ clinical information, such as histopathologic findings or the surgical procedure that was used. SSTMs were interpreted as malignant or non-malignant considering the following imaging features: mass lobulation, fascial edema, skin thickening, skin contact, hemorrhage, or necrosis. An obtuse angle between a mass and the superficial investing fascia and the mass crossing the fascia were also considered as
B
JR
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
signs suggesting malignancy 1,7,9,10. The lesion size was assessed according to the longest diameter measurement. However, the readers did not take the lesion size into account as a significant criterion for differentiating between a non-malignant and malignant SSTMs 1. The same radiologists evaluated the combined sets of conventional MR and axial DW imaging at least 120 days after the first evaluation in random order. To assess the DW imaging features of malignant SSTMs, both readers independently analyzed the qualitative signal intensity pattern on DW images and the quantitative ADC value of
SSTMs in a blinded fashion. On qualitative analysis, the signal intensity of SSTMs on DW images using b-values of 0, 400 and 800 sec/mm2 was classified into three grades, in which grade 0 = signal intensity gradually decreased as the b-value increased,
FS
grade 1 = little or no change in signal intensity was shown as the b-value increased, and grade 2 = signal intensity gradually increased as the b-value increased. DWI scans were windowed by the readers to determine
the visually optimal level to clearly outline the margin of the mass from the surrounding tissue. We assumed that
O
the lesions would be malignant when visually more increased signal intensity was shown with increasing b-
O
values on DW imaging 4,11.
For quantitative analysis, in the case of inhomogeneous SSTMs, both mean ADC values were obtained from an
R
entire mass (ADCentire) on one representative axial plane and enhancing solid portion (ADCsolid) that manifested
P
with hyperintense signal on DW images with a high b-value. The ADC value was measured with use of manually drawn ROIs on the ADC map and the average value inside the ROI (mean ADC) was recorded . The
D
region was determined to be the solid portion when it was hyperintense on T2-weighted images, hypointense on T1-weighted images, and enhanced on fat-suppressed contrast-enhanced T1-weighted images. ADCentire was
E
obtained from ROI drawing the entire mass on one axial plane in which the tumor section with the largest
effects
4,12
C T
diameter on conventional MRI. The peripheral most portions was excluded in order to avoid partial-volume . To draw the proper ROI in the representative region of a mass, each reader performed side-by-side
comparison between the DW images and the corresponding standard MR images (Fig 1). ADCs were measured
R R E
with combinations of three b-values (0, 400, and 800sec/mm2). As for the SSTM showing homogenous enhancement, there was no need to measure separately ADC value as there was little difference between ADCentire (1380.2±506.8) and ADCsolid (1325.6±497.5).
O
Statistical Analysis
C
Statistical analysis was performed using commercial software (SPSS version 21: [SPSS, Chicago, IL, USA] and
N
Medcalc, version 11.3.0.0 [Medcalc, Mariakerke, Belgium]). For all tests, P
© 2016 The Authors. Published by the British Institute of Radiology
Usefulness of Diffusion-Weighted MR Imaging for Differentiating between Benign and
FS
Malignant Superficial Soft Tissue Tumors and Tumor-like Lesions
O
Ji Young Jeon, M.D., Hye Won Chung, M.D., Min Hee Lee, M.D., Sang Hoon Lee, M.D., Myung Jin
O
Shin, M.D.
Department of Radiology and Research Institute of Radiology, University of Ulsan College of
P
R
Medicine, Asan Medical Center
D
Ji Young Jeon, M.D.: First author
C T
E
E-mail: [email protected]
Min Hee Lee, M.D. : [email protected]
R R E
Sang Hoon Lee, M.D.: [email protected]
U
N
C
O
Myung Jin Shin, M.D. : [email protected]
Address to Correspondence: Hye Won Chung, M.D.
B
JR
Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center, 88, Olympic-Ro 43-Gil, Songpa-Gu Seoul 138-736, Korea e-mail: [email protected]
Objectives: To evaluate the usefulness of adding DW imaging with ADC mapping to conventional 3.0-T MR imaging to differentiate between benign and malignant superficial soft tissue masses (SSTMs). Methods: The institutional review board approved this study and informed consent was waived. The authors
FS
retrospectively analyzed conventional MR images including DW images (b-values: 0, 400, 800sec/mm2) in 60 histologically proven SSTMs (35 benign; 25 malignant) excluding lipomas. Two radiologists independently evaluated the conventional MRI alone and again with the additional DWI for evaluation of malignant masses.
B
O
The mean ADC values measured within an entire mass and the contrast enhancing solid portion were used for
O
quantitative analysis. Diagnostic performances were compared using ROC analysis.
Results: For an inexperienced reader, using only conventional MRI, sensitivity, specificity and accuracy were
R
84%, 80% and 81.6%, respectively. When combining conventional MRI and DWI, the sensitivity, specificity
P
and accuracy were 96%, 85.7% and 90%, respectively. Additional DWI influenced the improvement of the rate of correct diagnosis by 8.3% (5/60). For an experienced reader, additional DWI revealed the same accuracy of
D
86.7% without added value on the correct diagnosis. The group mean ADCs of malignant SSTMs was significantly lower than that of benign SSTM (P< .001). The best diagnostic performance with respect to
E
differentiation of SSTMs could be obtained when conventional MR imaging was assessed in combination with
C T
DW imaging.
Conclusions: Adding qualitative and quantitative DWI to conventional MR imaging can improve the diagnostic performance for differentiation between benign and malignant SSTMs.
R R E
.
Advances in knowledge: Because the imaging characteristics of many malignant superficial soft tissue lesions overlap with those of benign ones, inadequate surgical resection due to misinterpretation of MR imaging often occurs. Adding diffusion-weighted imaging to conventional MR imaging yields greater diagnostic performances
O
(area under the receiver operating characteristic curve [AUC], 0.83–0.99) than does use of conventional MR
N
C
imaging alone (AUC, 0.71–0.93) in the evaluation of malignant superficial masses by inexperienced readers.
U
Key Words:
Superficial soft-tissue masses, Magnetic resonance imaging, diffusion, ADC, Malignant superficial soft-tissue tumors
JR
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
Abbreviations: ADC = apparent diffusion coefficient DW = diffusion-weighted
ROC = receiver operating characteristic
FS
ROI = region of interest
Superficial soft-tissue masses are a common reason for visiting the outpatient clinics. As the availability of radiologic imaging has expanded, the chance of encountering any superficial soft tissue masses (SSTMs) for
O
radiologists has also been increased. In the case of some SSTMs, such as lipomas, a definitive diagnosis is not
B
O
difficult using conventional MR imaging only because of their characteristic fatty component. However, in much clinical practice, the differentiation between benign and malignant SSTMs using only conventional MR problematic as many of their imaging features are nonspecific and some overlap exists between the
R
imaging is
P
malignant and benign groups 1. Diffusion-weighted imaging (DWI) measures the random motion of water protons in tissue. The random Brownian motion of water protons determines DWI signal intensity, and the quantitative assessment of water diffusion in tissues is expressed as the apparent diffusion coefficient (ADC)
assessing soft tissue tumors have been widely investigated
2,3
. Although the usefulness of DW imaging for
E
tissue from that attained using conventional MR techniques
D
values. Because of this, the diffusion-weighted (DW) procedure provides different tissue contrast about diseased 2,4-6
, there are not many publications that separately
C T
evaluating the usefulness of DW imaging for superficial soft tissue masses. The purpose of our study is to retrospectively determine specifically the value of adding DW imaging with ADC mapping to conventional 3.0-
R R E
T magnetic resonance imaging to differentiate between benign and malignant SSTMs.
Materials and Methods
O
Patient population
C
Our institutional review board approved this study, and waived the requirement for informed consent.
N
Since August 2013, MR imaging that included axial DW imaging at 3.0-T has been performed for soft tissue masses at our institution. From August 2013 to April 2015, all of the consecutive patients who underwent MR
U
imaging with DW imaging for evaluation of soft tissue masses localized to the trunk or the extremities, were retrospectively evaluated. Two hundred and thirty two patients were identified on the initial survey. One hundred and thirty-eight patients did not undergo histopathological confirmation and were thus excluded from
JR
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
our study.
The 94 patients remaining with superficially located lesions were further filtered for image quality,
previous excision/surgery and size as well as pathology indicating lipoma by a radiologist (J.Y.J.) with two years of experience in musculoskeletal radiology. SSTMs were defined as lesions located within the subcutaneous fat, and superficial to the superficial investing fascia, which separates the subcutaneous tissue layer from the underlying muscle on conventional MR imaging 1,7. Fourteen patients were excluded due to : image distortion of DW imaging (n= 6), previous treatment such as excision or excisional biopsy (n=5), and lesions less than 5mm in maximum diameter, as these were too small to further characterize on conventional MR imaging (n =3). Patients were also excluded who had lipomas (n =20) determined on pathologic confirmation. Finally, a total of
60 patients (mean age, 48.5 years; age range, 5–80 years; 30 men [mean age, 47.2 years; age range, 5–80 years] and 30 women [mean age, 49.8 years; age range, 14–71 years]) with SSTMs were included in our study. The
FS
detailed histopathologic diagnoses are listed in Table 1.
O
MR Imaging Protocols
All examinations were performed on a 3-T scanner (Achieva; Philips Medical Systems, Best, the Netherlands)
O
system. Depending on the localization of the tumor, dedicated surface coils were used. The conventional MR imaging protocols included axial T1-weighted turbo spin-echo (TSE) sequence, axial T2-weighted TSE
R
sequences with and without fat suppression, coronal or sagittal T1-weighted TSE sequence, and coronal or
P
sagittal T2-weighted TSE sequence with and without fat suppression. In all 60 patients, axial, coronal, and sagittal fat-suppressed contrast–enhanced T1-weighted sequences were also performed. Before the commencement of this diffusion MR study, a series of image quality tests were performed to adjust acquisition
D
parameters of diffusion and total scan time. A single-shot spin-echo echo-planar DW sequence was performed in
E
axial planes. A parallel imaging technique using sensitivity encoding, or SENSE, was combined with an acceleration factor of 1.5. The echo-planar imaging factor was 67, and sensitizing diffusion gradients were
C T
applied sequentially in the x, y, and z directions with b values of 0, 400, and 800 sec/mm 2 8. The ADC maps were automatically calculated using commercial software and were included in the sequences. The sequence
MR Imaging Analysis
R R E
parameters are presented in Table 2.
O
To assess the added value of DW imaging in the differentiation of malignant from nonmalignant superficial soft tissue lesions, the diagnostic performance of conventional MR imaging alone and additional DW imaging with
C
ADC mapping was compared. To evaluate conventional MR imaging alone, two musculoskeletal radiologists (H.W.C., J.Y.J.; 19-years and 2-years of clinical experience in musculoskeletal MR imaging, respectively)
N
independently reviewed the conventional MR images of 60 patients, both being unaware of the previous
U
imaging reports and the patients’ clinical information, such as histopathologic findings or the surgical procedure that was used. SSTMs were interpreted as malignant or non-malignant considering the following imaging features: mass lobulation, fascial edema, skin thickening, skin contact, hemorrhage, or necrosis. An obtuse angle between a mass and the superficial investing fascia and the mass crossing the fascia were also considered as
B
JR
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65
signs suggesting malignancy 1,7,9,10. The lesion size was assessed according to the longest diameter measurement. However, the readers did not take the lesion size into account as a significant criterion for differentiating between a non-malignant and malignant SSTMs 1. The same radiologists evaluated the combined sets of conventional MR and axial DW imaging at least 120 days after the first evaluation in random order. To assess the DW imaging features of malignant SSTMs, both readers independently analyzed the qualitative signal intensity pattern on DW images and the quantitative ADC value of
SSTMs in a blinded fashion. On qualitative analysis, the signal intensity of SSTMs on DW images using b-values of 0, 400 and 800 sec/mm2 was classified into three grades, in which grade 0 = signal intensity gradually decreased as the b-value increased,
FS
grade 1 = little or no change in signal intensity was shown as the b-value increased, and grade 2 = signal intensity gradually increased as the b-value increased. DWI scans were windowed by the readers to determine
the visually optimal level to clearly outline the margin of the mass from the surrounding tissue. We assumed that
O
the lesions would be malignant when visually more increased signal intensity was shown with increasing b-
O
values on DW imaging 4,11.
For quantitative analysis, in the case of inhomogeneous SSTMs, both mean ADC values were obtained from an
R
entire mass (ADCentire) on one representative axial plane and enhancing solid portion (ADCsolid) that manifested
P
with hyperintense signal on DW images with a high b-value. The ADC value was measured with use of manually drawn ROIs on the ADC map and the average value inside the ROI (mean ADC) was recorded . The
D
region was determined to be the solid portion when it was hyperintense on T2-weighted images, hypointense on T1-weighted images, and enhanced on fat-suppressed contrast-enhanced T1-weighted images. ADCentire was
E
obtained from ROI drawing the entire mass on one axial plane in which the tumor section with the largest
effects
4,12
C T
diameter on conventional MRI. The peripheral most portions was excluded in order to avoid partial-volume . To draw the proper ROI in the representative region of a mass, each reader performed side-by-side
comparison between the DW images and the corresponding standard MR images (Fig 1). ADCs were measured
R R E
with combinations of three b-values (0, 400, and 800sec/mm2). As for the SSTM showing homogenous enhancement, there was no need to measure separately ADC value as there was little difference between ADCentire (1380.2±506.8) and ADCsolid (1325.6±497.5).
O
Statistical Analysis
C
Statistical analysis was performed using commercial software (SPSS version 21: [SPSS, Chicago, IL, USA] and
N
Medcalc, version 11.3.0.0 [Medcalc, Mariakerke, Belgium]). For all tests, P
