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The benefits of comparing conventional sonography, real-time spatial compound sonography, tissue harmonic sonography, and tissue harmonic compound sonography of hepatic lesions
Clinical Imaging 32 (2008) 11 – 15
The benefits of comparing conventional sonography, real-time spatial compound sonography, tissue harmonic sonography, and tissue harmonic compound sonography of hepatic lesions Chin-Lan Yen a , Chin-Ming Jeng a,⁎, Sien-Sing Yang b a Department of Radiology, Cathay General Hospital, Taipei, Taiwan Department of Internal Medicine, Cathay General Hospital, Taipei, Taiwan
b
Received 1 June 2007; accepted 1 July 2007
Abstract This study aimed to compare conventional sonography, tissue harmonic imaging (THI), spatial compound sonography (SONOCT), and SONOCT+THI for overall image quality, lesion conspicuity, and elimination of artifacts of hepatic lesions. Forty-five patients were randomly selected, and 51 different hepatic lesions were scanned using each of the four techniques. The combined images of SONOCT+THI exhibited the best image quality for solid and cystic lesions, while conventional images were the worst for most hepatic lesions (P b.001). SONOCT was the best for fatty liver. © 2008 Elsevier Inc. All rights reserved. Keywords: Spatial compound sonography; Tissue harmonic imaging; Hepatic lesions; Techniques; Fatty liver
1. Introduction Sonography is a well-known imaging modality because of its accessibility, cost-effectiveness, and lack of radiationinduced harm. It is recognized as the first choice of imaging techniques for evaluating abdominal and pelvic lesions. Nevertheless, there are still many unwanted artifacts that degrade the sensitivity and specificity of conventional sonography. Hence, there is a need to upgrade imaging techniques to overcome these undesired artifacts. Real-time spatial compound sonography (SONOCT) and tissue harmonic imaging (THI) are two new sonographic techniques that were developed in recent decades to improve overall image quality and eliminate unwanted artifacts [1].
⁎ Corresponding author. Department of Radiology, Cathay General Hospital, Taipei 10650, Taiwan. Tel.: +886 2 27082121x3861; fax: +886 2 23932877. E-mail address: [email protected] (C.-M. Jeng). 0899-7071/08/$ – see front matter © 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.clinimag.2007.07.002
SONOCT is a state-of-the-art sonographic technique for reducing clutter and speckle artifacts, which will eventually improve image quality. The concept of real-time spatial compounding sonography was around as early as the 1960s, but renewed interest arose in the 1990s as computed beamsteering technology was introduced. Conventional real-time sonography emits sound beams from the scan head, which strike the anatomical structure and return to the scan head. SONOCT uses electronic beam steering of a transducer array and as many as nine scans of an object, which are acquired from different view angles, merged in overlapping fashion, and averaged to form a compound real-time image. Generating an image from multiple scanning lines that strike the target from different angles results in better delineated margins, reduces image artifacts and noise, and enhances image contrast. Reports of many studies have concluded that SONOCT improves image quality of musculoskeletal, breast, vascular, and skin lesions significantly [2–6]. THI is based on nonlinear distortion of an acoustic signal as it travels through the body. The ultrasound harmonics are
12
C.-L. Yen et al. / Clinical Imaging 32 (2008) 11–15
generated by tissue or by contrast agents. Contrast-agent harmonics are generated by reflections from the injected contrast agent. When no contrast is employed, harmonics are generated by the tissue itself as a result of the distal propagation of the fundamental (transmitted) band. The fundamental band consists of echoes produced by tissue interfaces and inhomogeneity, whereas the harmonic band is generated by the tissue itself. Most harmonic imaging is currently performed by using the second harmonic component. The following are the theoretical advantages of THI: (a) it improves signal-to-noise ratio; (b) it improves spatial resolution; and (c) it improves visualization of tissue depth. The resulting increase in contrast and resolution can lead to a more confident assessment of abdominal and pelvic masses, especially in obese patients, differentiating hypoechoic solid masses and cystic lesions [7–11]. Combined images from SONOCT and THI on abdominal and pelvic lesions provide the best overall image quality, best lesion conspicuity, and fewest artifacts [1,12]. Our study was designed to compare four sonographic techniques—conventional sonography, THI alone, SONOCT alone, and SONOCT+THI—for overall image quality, lesion conspicuity, and elimination of artifacts from hepatic lesions.
2. Materials and methods 2.1. Patients We evaluated 45 patients including 26 females and 19 males whose average age was 52 years (range, 32–82). Our study was conducted from February to May 2006. Fifty-one different hepatic lesions were collected randomly, including hyperechoic hemangioma (37%), hepatic cysts (23%), calcifications (14%), and fatty liver (25%). The data for these patients, who were able to tolerate a deep breath-hold for us to catch the four different images simultaneously, were collected from the health care center. Hepatic hemangiomas were selected to represent solid lesions because they are common findings in the health care center. All the lesions are confirmed by CT scan, and ultrasound follow-up studies at intervals of 3, 6, and 12 months made the diagnosis highly probable [13–16]. All patients had given informed consent, and the study was approved by our hospital's Research Ethics Committee. 2.2. Ultrasound unit and imaging protocol We used a Philips HD11 Ultrasound System (distributed by Philips Medical Systems, Andover, MA, USA) with a 2- to 5-MHz convex transducer. We scanned each lesion by each of the four different sonographic techniques in the following order: SONOCT+THI, SONOCT alone, THI alone, and, finally, conventional sonography. A single convex transducer was used, and the images were scanned by a single radiologist. A single switch on the control panel of the
console was used to alternate between the different imaging modes as each lesion was scanned. The ultrasound plane of section was maintained as constant as possible to catch the four different images simultaneously. Imaging parameters and instrument settings were not adjusted between different modes except for the gain setting, which was optimized for each image by the radiologist who was performing the examination. There are two kinds of SONOCT modes— survey (beam steering with five overlapping images) and target (nine overlapping images)—that can be selected. We used target mode for this study as the image quality could be maximized. 2.3. Image interpretation and data analysis Images were stored digitally in an ultrasound system and in the Picture Archiving and Communication System as well. Images of different hepatic lesions were evaluated side by side on the computer monitor by two different experienced radiologists who were unaware of the different sonographic techniques used. They scored images for overall quality, lesion conspicuity, and elimination of artifacts. Overall image quality was defined through a general assessment encompassing spatial resolution or detail, contrast of solid and fluid-filled structures, and absence of noise. Lesion conspicuity was defined as the visibility and clarity of the lesion (compared with adjacent structures) and the distinctness of posterior echo acoustic artifacts, which was considered useful. Artifacts including speckling, sidelobes, reverberation, and clutter and blurring degraded image quality. For all lesions, overall image quality, lesion conspicuity, and elimination of unwanted artifacts were assessed and categorized by grade. Observers independently graded the images from 1 (indicating the worst image) to 4 (indicating the best image). For statistical analysis, a single radiologist obtained all images, which were then evaluated by another experienced radiologist for overall image quality, lesion conspicuity, and unwanted artifacts. These were assessed and categorized from Grade 1 to Grade 4. The grader was blind to the sonographic technique used to produce each image. A Friedman test was used for multiple statistical comparisons between the four techniques. To make paired comparisons between different imaging modes, we used the Wilcoxon signed-rank test. Kappa scores were calculated to assess interobserver agreement. Statistical analysis was performed with a commercially available statistical software program (SPSS 11.0, Chicago, IL), and P value b .05 was considered significant.
3. Results The mean kappa score for the two independent observers was 0.336 (range, 0.046–1.000) and reflected moderate interobserver agreement. Mean scores for each
.009
b .00
b .00
2.9 (2.8–3.1) 1.0 (1.0–1.0) 1.6 (0.8–2.3) 1.5 (1.1–1.8) 2.7 (2.6–3.0) 1.9 (1.3–2.2) .774
b .001
.001
b .001
Calcification (n=7)
Abbreviations: CCT, combined image with SONOCT and tissue harmonic; SCT, SONOCT; THM, tissue harmonic; CSN, conventional sonography.
4.0 (4.0–4.0) 2.3 (2.0–2.6) 3.7 (3.3–4.2) .001
2.9 (2.8–3.1) 1.0 (1.0–1.0) 2.4 (1.7–3.2) 1.4 (1.1–1.7) 2.9 (2.7–3.1) 2.9 (2.0–3.7) 4.0 (4.0–4.0) 2.1 (1.9–2.3) 2.1 (0.8–3.5) 1.7 (1.3–2.1) 4.0 (4.0–4.0) 2.6 (1.3–3.9) .001
2.8 (2.6–3.1) 1.0 (1.0–1.0) 1.1 (0.8–1.5) 4.0 (4.0–4.0) 2.3 (2.0–2.6) 3.4 (2.9–3.9) 1.8 (1.4–2.3) 4.0 (4.0–4.0) 3.6 (3.1–4.1)
1.3 (1.0–1.6) 2.7 (2.4–3.0) 1.9 (1.5–2.2)
3.0 (3.0–3.0) 4.0 (4.0–4.0)
2.0 (2.0–2.0)
1.0 (1.0–1.0)
.007
4.0 (4.0–4.0)
3.0 (3.0–3.0)
4.0 (4.0–4.0) .011 1.3 (0.5–2.0)
1.6 (1.2–2.0) 4.0 (4.0–4.0) 2.8 (1.6–3.9)
.007 1.0 (1.0–1.0) 2.0 (2.0–2.0)
b .00
1.8 (1.0–2.5)
3.0 (3.0–3.0)
CSN
1.2 (1.0–1.3) 1.8 (1.7–2.0)
THM
3.8 (3.6–4.0) b .001 1.1 (1.0–1.3) 2.2 (1.9–2.5)
SCT CCT P value CSN THM
2.8 (2.5–3.2) 3.8 (3.7–4.0) b .001 1.1 (1.0–1.3)
CSN THM
1.9 (1.8–2.1) 3.1 (2.9–3.3)
SCT
3.8 (3.7–4.0)
Hyperechoic lesions (n=19) Hypoechoic lesions (n=4) Fatty liver (n=13) Cyst (n=12)
SCT CCT P value CCT
Elimination of artifacts Lesion conspicuousness Overall image quality
Lesion group
Table 1 Mean scores (95% confidence interval) for the four imaging techniques for different lesion groups
3.2 (3.0–3.4)
P value
C.-L. Yen et al. / Clinical Imaging 32 (2008) 11–15
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sonographic technique for overall image quality, lesion conspicuity, and elimination of unwanted artifacts were calculated and compared using a Friedman test (Table 1). SONOCT+THI was best for overall image quality, lesion conspicuity, and elimination of undesired artifacts of hyperechoic hemangiomas and cystic hepatic lesions, while conventional sonography was the worst (P b.001; Table 1). For example, for hyperechoic hemangiomas (Fig. 1), the combined SONOCT+THI image showed the best lesion conspicuity, while conventional imaging obscured smaller lesions and showed poor delineation of larger hepatic lesions. SONOCT was better for depiction of solid lesions, while THI was relatively better for cystic lesions (Pb.001). SONOCT was best for fatty infiltration, especially severe fatty liver, as it provided the utmost penetration, while THI was the worst for fatty liver (P b.001; Fig. 2). Lesion conspicuity of hepatic calcifications was indistinct (P=.721), although SONOCT+THI provided better image quality and eliminated unwanted artifacts.
4. Discussion SONOCT has been used since the earliest days of ultrasound imaging to reduce random noise known as “speckle,” which gives a granular appearance to an otherwise homogeneous region of tissue, and “clutter,” which arises from sidelobes, grating lobes, multipath reverberation, and other acoustical phenomena [2,3]. Several overlapping scans of an object are acquired from different view angles and then combined (usually by averaging) to form a compound image, which is made possible by computed beam-steering technology. Multiangle imaging studies have been shown not only to improve image quality but also to reduce speckle artifacts. Harmonics in ultrasound are generated by tissues or by contrast agents. Contrast-agent harmonics are generated by reflections from the injected contrast agent and not from the reflections from tissues. The nonlinear properties of microbubbles, which resonate when insonified, produce fundamental and harmonic frequency bands. When no contrast is employed, harmonics are generated by the tissue itself as a result of the distal propagation of the fundamental (transmitted) band. When a transducer sends a band of frequencies that have a certain characteristic center frequency, for example, 2 MHz, the returned frequencies will be in two or more frequency bands or spectra. The first corresponds to the transmitted fundamental band centered at 2 MHz and the second is the second harmonic band centered at 4 MHz [10]. With currently available equipment, the second harmonic is used for imaging. This approach requires a controlled ultrasonic spectrum that allows separation of the fundamental and harmonic frequencies. Harmonic sonography has the potential for improving image quality. The shorter wavelength of the harmonic
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C.-L. Yen et al. / Clinical Imaging 32 (2008) 11–15
SONOCT is the best sonographic technique for fatty infiltration, while THI is the worst. For patients with diffuse fatty infiltration in the liver, penetration of the ultrasound beam was better on conventional ultrasound than on harmonic imaging [7]. Various sources of harmonic leakage, including transmit waveform, signal bandwidth, and system nonlinearity, were investigated using both simulations and hydrophone measurements. Results indicated that sidelobe levels of the harmonic beam pattern were directly affected by harmonic leakage when the harmonic signal was obtained by filtering out the fundamental signal. Accurate control of the frequency content of the waveform prior to propagation is necessary to optimize imaging performance of the THI. The pulse inversion technique effectively suppresses harmonic leakage at the cost of imaging frame rate and potential motion artifacts [17]. SONOCT is relatively superior for evaluation of solid hepatic lesions, while THI is better for cystic lesions (Table 1). Kim et al. [12] had reported similar results as ours. The target mode (beam steering with nine overlapping images) of SONOCT may show better lesion conspicuity than the survey mode (five overlapping images), but it needs
Fig. 1. Comparison of hyperechoic hemangiomas detected by different sonographic modalities. (A) Combined images from harmonic and SONOCT techniques; (B) SONOCT-alone image; (C) harmonic-alone image; (D) conventional image. The combined image shows the best depiction of hyperechoic hepatic hemangiomas (including both bigger and smaller nodules), the least artifact, and the best image quality. The conventional image shows the worst image quality as its speckle artifact can easily obscure smaller lesions and only poorly delineate bigger nodules.
frequency provides better axial resolution, and the narrowed beam width improves lateral resolution as well. The harmonic signal is generated within tissues; hence, artifacts from the body wall may be less pronounced with tissue harmonic sonography. Image noise from scatter and sidelobe artifacts may also be diminished because of the harmonics generated by the transmitted pulse. Early reports indicated that the improved resolution and improved signal-to-noise ratio of THI render this technique particularly suitable for imaging technically difficult and obese patients [9]. The combination of SONOCT and THI theoretically summates the overall image quality of both of these two imaging techniques. Oktar et al. [1] introduced tissue harmonic compound sonography, which provided the best overall image quality, best lesion conspicuity, and fewest artifacts in abdominal and pelvic scanning. From our study, we conclude that SONOCT+THI produces the best delineation of most hepatic lesions except for fatty liver (Fig. 2).
Fig. 2. Comparison of fatty liver detected by different sonographic modalities. (A) Combined image using harmonic and SONOCT techniques; (B) SONOCT-alone image; (C) harmonic-alone image; (D) conventional image. SONOCT and conventional images are better for fatty liver study; the SONOCT image remains the best owing to diminished speckle artifact. The harmonic image and combined image show poor penetration for fatty infiltration; thus, the images are dark and blurred.
C.-L. Yen et al. / Clinical Imaging 32 (2008) 11–15
much more patience and longer times to collect the best images or else the images can easily be blurred by motion artifacts. Increases in the gain setting for SONOCT+THI are necessary as the images are usually “darker” than those from SONOCT alone. The posterior echo acoustic artifacts of the cystic and calcified lesions can be diminished by SONOCT, but SONOCT+THI recovered posterior echo acoustic artifacts as those were considered diagnostic figures of cystic and calcified lesions. Lesion conspicuity of calcifications was unsatisfactory (P=.721). THI was not beneficial for the evaluation of hepatic calcifications [11]. It is most probably due to different contents of calcifications. Hence, alternative selection of the imaging techniques is important or the calcifications or stones could be missed by only one of the imaging techniques. Alternative use of combined techniques of SONOCT+THI and SONOCT alone is an unavoidable selection. SONOCT+THI is a very sensitive sonographic imaging technique for the depiction of most hepatic lesions as it maximizes the advantages of both SONOCT and THI. The smooth images of SONOCT+THI are very helpful for lesion conspicuity. Although most sonographers are not trained to use this combined technique, we still recommend it for the whole course of the examination except for fatty liver. In conclusion, tissue harmonic compound sonography shows the best image quality, best lesion conspicuity, and the least artifacts for both solid and cystic hepatic lesions. Real-time SONOCT shows the best image quality for the fatty infiltration. References [1] Oktar SÖ, Yücel C, Özdemir H, Ulutürk A, Isik S. Comparison of conventional sonography, real-time compound sonography, tissue harmonic sonography, and tissue harmonic compound sonography of abdominal and pelvic lesions. AJR Am J Roentgenol 2003;181: 1341–7. [2] Entrekin RR, Porter BA, Sillesen HH, Wong AD, Cooperberg PL, Fix CH. Real-time spatial compound imaging: application to breast, vascular, and musculoskeletal ultrasound. Semin Ultrasound CT MR 2001;22:50–64. [3] Huber S, Wagner M, Medl M, Czembirek H. Real-time spatial compound imaging in breast ultrasound. Ultrasound Med Biol 2002;28:155–63.
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[4] Kofoed SC, Gronholdt ML, Wilhjelm JE, Bismuth J, Sillesen H. Realtime spatial compound imaging improves reproducibility in the evaluation of atherosclerotic carotid plaques. Ultrasound Med Biol 2001;27:1311–7. [5] Lin DC, Nazarian LN, O'Kane PL, McShane JM, Parker L, Merritt CRB. Advantages of real-time spatial compound sonography of the musculoskeletal system versus conventional sonography. AJR Am J Roentgenol 2002;179:1629–31. [6] Wortsman XC, Holm EA, Wulf HC, Jemec GBE. Real-time spatial compound ultrasound imaging of skin. Skin Res Technol 2004;10: 23–31. [7] Choudhry S, Gorman B, Charboneau W, Tradup DJ, Beck RJ, Kofler JM, Groth DS. Comparison of tissue harmonic imaging with conventional US in abdominal disease. Radiographics 2000;20: 1127–35. [8] Desser TS, Jeffrey RB, Lane MJ, Rails PW. Tissue harmonic imaging: utility in abdominal and pelvic sonography. J Clin Ultrasound 1999; 27:135–42. [9] Hann LE, Bach AM, Cramer LD, Siegel D, Yoo HH, Garcia R. Hepatic sonography: comparison of tissue harmonic and standard sonography techniques. AJR Am J Roentgenol 1999;173:201–6. [10] Tranquart F, Grenier N, Eder V, Pourcelot L. Clinical use of ultrasound tissue harmonic imaging. Ultrasound Med Biol 1999;25:889–94. [11] Yucel C, Ozdemir H, Asik E, Oner Y, Isik S. Benefits of tissue harmonic imaging in the evaluation of abdominal and pelvic lesions. Abdom Imaging 2003;28:103–9. [12] Kim SH, Lee JM, Kim KG, Kim JH, Han JK, Lee JY, Choi BI. Comparison of fundamental sonography, tissue-harmonic sonography, fundamental compound sonography, and tissue-harmonic compound sonography for focal hepatic lesions. Eur Radiol 2006;16: 2444–53. [13] Ricci OE, Fanfani S, Calabro A, Milano M, Ciatti S, Colagrande S, Masi A, Casini A, Acampora C, Ceccatel P. Diagnostic approach to hepatic hemangiomas detected by ultrasound. Hepatogastroenterology 1985;32:53–6. [14] Jacobs JE, Birnbaum BA, Shapiro MA, Langlotz CP, Slosman F, Rubesin SE, Horii SC. Diagnostic criteria for fatty infiltration of the liver on contrast-enhanced helical CT. AJR Am J Roentgenol 1998;171:659–64. [15] Schneider HT, Ell C, Benninger J, Theobaldy S, Friedel N, Rodl W, Heyder N, Hahn EG. Imaging procedures prior to the extracorporeal shockwave lithotripsy of gallstones. Dtsch Med Wochenschr 1991;116: 128–33. [16] Federle MP, Filly RA, Moss AA. Cystic hepatic neoplasms: complementary roles of CT and sonography. AJR Am J Roentgenol 1981;136:345–8. [17] Shen CC, Li PC. Harmonic leakage and image quality degradation in tissue harmonic imaging. IEEE Trans Ultrason Ferroelectr Freq Control 2001;48:728–36.
The benefits of comparing conventional sonography, real-time spatial compound sonography, tissue harmonic sonography, and tissue harmonic compound sonography of hepatic lesions Chin-Lan Yen a , Chin-Ming Jeng a,⁎, Sien-Sing Yang b a Department of Radiology, Cathay General Hospital, Taipei, Taiwan Department of Internal Medicine, Cathay General Hospital, Taipei, Taiwan
b
Received 1 June 2007; accepted 1 July 2007
Abstract This study aimed to compare conventional sonography, tissue harmonic imaging (THI), spatial compound sonography (SONOCT), and SONOCT+THI for overall image quality, lesion conspicuity, and elimination of artifacts of hepatic lesions. Forty-five patients were randomly selected, and 51 different hepatic lesions were scanned using each of the four techniques. The combined images of SONOCT+THI exhibited the best image quality for solid and cystic lesions, while conventional images were the worst for most hepatic lesions (P b.001). SONOCT was the best for fatty liver. © 2008 Elsevier Inc. All rights reserved. Keywords: Spatial compound sonography; Tissue harmonic imaging; Hepatic lesions; Techniques; Fatty liver
1. Introduction Sonography is a well-known imaging modality because of its accessibility, cost-effectiveness, and lack of radiationinduced harm. It is recognized as the first choice of imaging techniques for evaluating abdominal and pelvic lesions. Nevertheless, there are still many unwanted artifacts that degrade the sensitivity and specificity of conventional sonography. Hence, there is a need to upgrade imaging techniques to overcome these undesired artifacts. Real-time spatial compound sonography (SONOCT) and tissue harmonic imaging (THI) are two new sonographic techniques that were developed in recent decades to improve overall image quality and eliminate unwanted artifacts [1].
⁎ Corresponding author. Department of Radiology, Cathay General Hospital, Taipei 10650, Taiwan. Tel.: +886 2 27082121x3861; fax: +886 2 23932877. E-mail address: [email protected] (C.-M. Jeng). 0899-7071/08/$ – see front matter © 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.clinimag.2007.07.002
SONOCT is a state-of-the-art sonographic technique for reducing clutter and speckle artifacts, which will eventually improve image quality. The concept of real-time spatial compounding sonography was around as early as the 1960s, but renewed interest arose in the 1990s as computed beamsteering technology was introduced. Conventional real-time sonography emits sound beams from the scan head, which strike the anatomical structure and return to the scan head. SONOCT uses electronic beam steering of a transducer array and as many as nine scans of an object, which are acquired from different view angles, merged in overlapping fashion, and averaged to form a compound real-time image. Generating an image from multiple scanning lines that strike the target from different angles results in better delineated margins, reduces image artifacts and noise, and enhances image contrast. Reports of many studies have concluded that SONOCT improves image quality of musculoskeletal, breast, vascular, and skin lesions significantly [2–6]. THI is based on nonlinear distortion of an acoustic signal as it travels through the body. The ultrasound harmonics are
12
C.-L. Yen et al. / Clinical Imaging 32 (2008) 11–15
generated by tissue or by contrast agents. Contrast-agent harmonics are generated by reflections from the injected contrast agent. When no contrast is employed, harmonics are generated by the tissue itself as a result of the distal propagation of the fundamental (transmitted) band. The fundamental band consists of echoes produced by tissue interfaces and inhomogeneity, whereas the harmonic band is generated by the tissue itself. Most harmonic imaging is currently performed by using the second harmonic component. The following are the theoretical advantages of THI: (a) it improves signal-to-noise ratio; (b) it improves spatial resolution; and (c) it improves visualization of tissue depth. The resulting increase in contrast and resolution can lead to a more confident assessment of abdominal and pelvic masses, especially in obese patients, differentiating hypoechoic solid masses and cystic lesions [7–11]. Combined images from SONOCT and THI on abdominal and pelvic lesions provide the best overall image quality, best lesion conspicuity, and fewest artifacts [1,12]. Our study was designed to compare four sonographic techniques—conventional sonography, THI alone, SONOCT alone, and SONOCT+THI—for overall image quality, lesion conspicuity, and elimination of artifacts from hepatic lesions.
2. Materials and methods 2.1. Patients We evaluated 45 patients including 26 females and 19 males whose average age was 52 years (range, 32–82). Our study was conducted from February to May 2006. Fifty-one different hepatic lesions were collected randomly, including hyperechoic hemangioma (37%), hepatic cysts (23%), calcifications (14%), and fatty liver (25%). The data for these patients, who were able to tolerate a deep breath-hold for us to catch the four different images simultaneously, were collected from the health care center. Hepatic hemangiomas were selected to represent solid lesions because they are common findings in the health care center. All the lesions are confirmed by CT scan, and ultrasound follow-up studies at intervals of 3, 6, and 12 months made the diagnosis highly probable [13–16]. All patients had given informed consent, and the study was approved by our hospital's Research Ethics Committee. 2.2. Ultrasound unit and imaging protocol We used a Philips HD11 Ultrasound System (distributed by Philips Medical Systems, Andover, MA, USA) with a 2- to 5-MHz convex transducer. We scanned each lesion by each of the four different sonographic techniques in the following order: SONOCT+THI, SONOCT alone, THI alone, and, finally, conventional sonography. A single convex transducer was used, and the images were scanned by a single radiologist. A single switch on the control panel of the
console was used to alternate between the different imaging modes as each lesion was scanned. The ultrasound plane of section was maintained as constant as possible to catch the four different images simultaneously. Imaging parameters and instrument settings were not adjusted between different modes except for the gain setting, which was optimized for each image by the radiologist who was performing the examination. There are two kinds of SONOCT modes— survey (beam steering with five overlapping images) and target (nine overlapping images)—that can be selected. We used target mode for this study as the image quality could be maximized. 2.3. Image interpretation and data analysis Images were stored digitally in an ultrasound system and in the Picture Archiving and Communication System as well. Images of different hepatic lesions were evaluated side by side on the computer monitor by two different experienced radiologists who were unaware of the different sonographic techniques used. They scored images for overall quality, lesion conspicuity, and elimination of artifacts. Overall image quality was defined through a general assessment encompassing spatial resolution or detail, contrast of solid and fluid-filled structures, and absence of noise. Lesion conspicuity was defined as the visibility and clarity of the lesion (compared with adjacent structures) and the distinctness of posterior echo acoustic artifacts, which was considered useful. Artifacts including speckling, sidelobes, reverberation, and clutter and blurring degraded image quality. For all lesions, overall image quality, lesion conspicuity, and elimination of unwanted artifacts were assessed and categorized by grade. Observers independently graded the images from 1 (indicating the worst image) to 4 (indicating the best image). For statistical analysis, a single radiologist obtained all images, which were then evaluated by another experienced radiologist for overall image quality, lesion conspicuity, and unwanted artifacts. These were assessed and categorized from Grade 1 to Grade 4. The grader was blind to the sonographic technique used to produce each image. A Friedman test was used for multiple statistical comparisons between the four techniques. To make paired comparisons between different imaging modes, we used the Wilcoxon signed-rank test. Kappa scores were calculated to assess interobserver agreement. Statistical analysis was performed with a commercially available statistical software program (SPSS 11.0, Chicago, IL), and P value b .05 was considered significant.
3. Results The mean kappa score for the two independent observers was 0.336 (range, 0.046–1.000) and reflected moderate interobserver agreement. Mean scores for each
.009
b .00
b .00
2.9 (2.8–3.1) 1.0 (1.0–1.0) 1.6 (0.8–2.3) 1.5 (1.1–1.8) 2.7 (2.6–3.0) 1.9 (1.3–2.2) .774
b .001
.001
b .001
Calcification (n=7)
Abbreviations: CCT, combined image with SONOCT and tissue harmonic; SCT, SONOCT; THM, tissue harmonic; CSN, conventional sonography.
4.0 (4.0–4.0) 2.3 (2.0–2.6) 3.7 (3.3–4.2) .001
2.9 (2.8–3.1) 1.0 (1.0–1.0) 2.4 (1.7–3.2) 1.4 (1.1–1.7) 2.9 (2.7–3.1) 2.9 (2.0–3.7) 4.0 (4.0–4.0) 2.1 (1.9–2.3) 2.1 (0.8–3.5) 1.7 (1.3–2.1) 4.0 (4.0–4.0) 2.6 (1.3–3.9) .001
2.8 (2.6–3.1) 1.0 (1.0–1.0) 1.1 (0.8–1.5) 4.0 (4.0–4.0) 2.3 (2.0–2.6) 3.4 (2.9–3.9) 1.8 (1.4–2.3) 4.0 (4.0–4.0) 3.6 (3.1–4.1)
1.3 (1.0–1.6) 2.7 (2.4–3.0) 1.9 (1.5–2.2)
3.0 (3.0–3.0) 4.0 (4.0–4.0)
2.0 (2.0–2.0)
1.0 (1.0–1.0)
.007
4.0 (4.0–4.0)
3.0 (3.0–3.0)
4.0 (4.0–4.0) .011 1.3 (0.5–2.0)
1.6 (1.2–2.0) 4.0 (4.0–4.0) 2.8 (1.6–3.9)
.007 1.0 (1.0–1.0) 2.0 (2.0–2.0)
b .00
1.8 (1.0–2.5)
3.0 (3.0–3.0)
CSN
1.2 (1.0–1.3) 1.8 (1.7–2.0)
THM
3.8 (3.6–4.0) b .001 1.1 (1.0–1.3) 2.2 (1.9–2.5)
SCT CCT P value CSN THM
2.8 (2.5–3.2) 3.8 (3.7–4.0) b .001 1.1 (1.0–1.3)
CSN THM
1.9 (1.8–2.1) 3.1 (2.9–3.3)
SCT
3.8 (3.7–4.0)
Hyperechoic lesions (n=19) Hypoechoic lesions (n=4) Fatty liver (n=13) Cyst (n=12)
SCT CCT P value CCT
Elimination of artifacts Lesion conspicuousness Overall image quality
Lesion group
Table 1 Mean scores (95% confidence interval) for the four imaging techniques for different lesion groups
3.2 (3.0–3.4)
P value
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sonographic technique for overall image quality, lesion conspicuity, and elimination of unwanted artifacts were calculated and compared using a Friedman test (Table 1). SONOCT+THI was best for overall image quality, lesion conspicuity, and elimination of undesired artifacts of hyperechoic hemangiomas and cystic hepatic lesions, while conventional sonography was the worst (P b.001; Table 1). For example, for hyperechoic hemangiomas (Fig. 1), the combined SONOCT+THI image showed the best lesion conspicuity, while conventional imaging obscured smaller lesions and showed poor delineation of larger hepatic lesions. SONOCT was better for depiction of solid lesions, while THI was relatively better for cystic lesions (Pb.001). SONOCT was best for fatty infiltration, especially severe fatty liver, as it provided the utmost penetration, while THI was the worst for fatty liver (P b.001; Fig. 2). Lesion conspicuity of hepatic calcifications was indistinct (P=.721), although SONOCT+THI provided better image quality and eliminated unwanted artifacts.
4. Discussion SONOCT has been used since the earliest days of ultrasound imaging to reduce random noise known as “speckle,” which gives a granular appearance to an otherwise homogeneous region of tissue, and “clutter,” which arises from sidelobes, grating lobes, multipath reverberation, and other acoustical phenomena [2,3]. Several overlapping scans of an object are acquired from different view angles and then combined (usually by averaging) to form a compound image, which is made possible by computed beam-steering technology. Multiangle imaging studies have been shown not only to improve image quality but also to reduce speckle artifacts. Harmonics in ultrasound are generated by tissues or by contrast agents. Contrast-agent harmonics are generated by reflections from the injected contrast agent and not from the reflections from tissues. The nonlinear properties of microbubbles, which resonate when insonified, produce fundamental and harmonic frequency bands. When no contrast is employed, harmonics are generated by the tissue itself as a result of the distal propagation of the fundamental (transmitted) band. When a transducer sends a band of frequencies that have a certain characteristic center frequency, for example, 2 MHz, the returned frequencies will be in two or more frequency bands or spectra. The first corresponds to the transmitted fundamental band centered at 2 MHz and the second is the second harmonic band centered at 4 MHz [10]. With currently available equipment, the second harmonic is used for imaging. This approach requires a controlled ultrasonic spectrum that allows separation of the fundamental and harmonic frequencies. Harmonic sonography has the potential for improving image quality. The shorter wavelength of the harmonic
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SONOCT is the best sonographic technique for fatty infiltration, while THI is the worst. For patients with diffuse fatty infiltration in the liver, penetration of the ultrasound beam was better on conventional ultrasound than on harmonic imaging [7]. Various sources of harmonic leakage, including transmit waveform, signal bandwidth, and system nonlinearity, were investigated using both simulations and hydrophone measurements. Results indicated that sidelobe levels of the harmonic beam pattern were directly affected by harmonic leakage when the harmonic signal was obtained by filtering out the fundamental signal. Accurate control of the frequency content of the waveform prior to propagation is necessary to optimize imaging performance of the THI. The pulse inversion technique effectively suppresses harmonic leakage at the cost of imaging frame rate and potential motion artifacts [17]. SONOCT is relatively superior for evaluation of solid hepatic lesions, while THI is better for cystic lesions (Table 1). Kim et al. [12] had reported similar results as ours. The target mode (beam steering with nine overlapping images) of SONOCT may show better lesion conspicuity than the survey mode (five overlapping images), but it needs
Fig. 1. Comparison of hyperechoic hemangiomas detected by different sonographic modalities. (A) Combined images from harmonic and SONOCT techniques; (B) SONOCT-alone image; (C) harmonic-alone image; (D) conventional image. The combined image shows the best depiction of hyperechoic hepatic hemangiomas (including both bigger and smaller nodules), the least artifact, and the best image quality. The conventional image shows the worst image quality as its speckle artifact can easily obscure smaller lesions and only poorly delineate bigger nodules.
frequency provides better axial resolution, and the narrowed beam width improves lateral resolution as well. The harmonic signal is generated within tissues; hence, artifacts from the body wall may be less pronounced with tissue harmonic sonography. Image noise from scatter and sidelobe artifacts may also be diminished because of the harmonics generated by the transmitted pulse. Early reports indicated that the improved resolution and improved signal-to-noise ratio of THI render this technique particularly suitable for imaging technically difficult and obese patients [9]. The combination of SONOCT and THI theoretically summates the overall image quality of both of these two imaging techniques. Oktar et al. [1] introduced tissue harmonic compound sonography, which provided the best overall image quality, best lesion conspicuity, and fewest artifacts in abdominal and pelvic scanning. From our study, we conclude that SONOCT+THI produces the best delineation of most hepatic lesions except for fatty liver (Fig. 2).
Fig. 2. Comparison of fatty liver detected by different sonographic modalities. (A) Combined image using harmonic and SONOCT techniques; (B) SONOCT-alone image; (C) harmonic-alone image; (D) conventional image. SONOCT and conventional images are better for fatty liver study; the SONOCT image remains the best owing to diminished speckle artifact. The harmonic image and combined image show poor penetration for fatty infiltration; thus, the images are dark and blurred.
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much more patience and longer times to collect the best images or else the images can easily be blurred by motion artifacts. Increases in the gain setting for SONOCT+THI are necessary as the images are usually “darker” than those from SONOCT alone. The posterior echo acoustic artifacts of the cystic and calcified lesions can be diminished by SONOCT, but SONOCT+THI recovered posterior echo acoustic artifacts as those were considered diagnostic figures of cystic and calcified lesions. Lesion conspicuity of calcifications was unsatisfactory (P=.721). THI was not beneficial for the evaluation of hepatic calcifications [11]. It is most probably due to different contents of calcifications. Hence, alternative selection of the imaging techniques is important or the calcifications or stones could be missed by only one of the imaging techniques. Alternative use of combined techniques of SONOCT+THI and SONOCT alone is an unavoidable selection. SONOCT+THI is a very sensitive sonographic imaging technique for the depiction of most hepatic lesions as it maximizes the advantages of both SONOCT and THI. The smooth images of SONOCT+THI are very helpful for lesion conspicuity. Although most sonographers are not trained to use this combined technique, we still recommend it for the whole course of the examination except for fatty liver. In conclusion, tissue harmonic compound sonography shows the best image quality, best lesion conspicuity, and the least artifacts for both solid and cystic hepatic lesions. Real-time SONOCT shows the best image quality for the fatty infiltration. References [1] Oktar SÖ, Yücel C, Özdemir H, Ulutürk A, Isik S. Comparison of conventional sonography, real-time compound sonography, tissue harmonic sonography, and tissue harmonic compound sonography of abdominal and pelvic lesions. AJR Am J Roentgenol 2003;181: 1341–7. [2] Entrekin RR, Porter BA, Sillesen HH, Wong AD, Cooperberg PL, Fix CH. Real-time spatial compound imaging: application to breast, vascular, and musculoskeletal ultrasound. Semin Ultrasound CT MR 2001;22:50–64. [3] Huber S, Wagner M, Medl M, Czembirek H. Real-time spatial compound imaging in breast ultrasound. Ultrasound Med Biol 2002;28:155–63.
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