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Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ
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ANL-1910; No. of Pages 6 Auris Nasus Larynx xxx (2014) xxx–xxx
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Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ Takashi Matsuzuka MD, PhD*, Masahiro Suzuki MD, Satoshi Saijo MD, Masakazu Ikeda MD, Takamichi Matsui MD, PhD, Yukio Nomoto MD, PhD, Mika Nomoto MD, PhD, Mitsuyoshi Imaizumi MD, PhD, Yasuhiro Tada MD, PhD, Koichi Omori MD, PhD Department of Otolaryngology, Fukushima Medical University School of Medicine, Japan
A R T I C L E I N F O
A B S T R A C T
Article history: Received 22 June 2014 Accepted 15 August 2014 Available online xxx
Objective: To evaluate normal salivary gland stiffness and compare the diagnostic performance of virtual touch quantification (VTQ) and virtual touch imaging quantification (VTIQ) for head and neck tumor. Methods: A total of 92 measurements were examined, comprising 77 normal salivary glands, 11 benign tumors and four malignant tumors. Examinations were made to evaluate normal salivary gland stiffness and compare the diagnostic performances of new ultrasonic techniques regarding head and neck tumor. Results: The mean values of VTQ and VTIQ for the normal salivary group (NSG) were 1.92 and 2.06 m/s, respectively. The VTQ and VTIQ values were correlative, and there were no statistical differences in each mean value between the normal parotid glands and submandibular glands. For the benign tumor group (BTG), four of the 11 values were non-numeric and were considered above the measurable range. The mean VTIQ value for the BTG was 4.24 m/s. For the malignant tumor group (MTG), all four VTQ values were non-numeric. The mean VTIQ value for the MTG was 6.52 m/s. For the mean VTIQ values, significant differences were observed among the three groups. The optimum VTQ cutoff value to detect malignant tumors was above the measurable range, and that of VTIQ was 4.83 m/s. Conclusion: The VTQ and VTIQ values were correlative for the salivary glands, and the stiffnesses of normal parotid glands were almost same as those of submandibular glands. VTQ and VTIQ values could be applied for the preoperative diagnosis in salivary gland lesions. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Normal salivary gland Head and neck tumor Salivary gland tumor Acoustic radiation force impulse (ARFI) Virtual touch tissue quantification (VTQ) Virtual touch tissue imaging quantification (VTIQ)
1. Introduction In salivary gland tumor, although most head and neck cancer is diagnosed pathologically with squamous cell carcinoma, there are various histopathological types, of which squamous cell carcinoma is rare. One of the most serious problems regarding salivary gland tumor is that many are difficult to identify as either benign or malignant before treatment. Due to the density of the cancer cells and blood vessels, the stiffness of the cancer tissue increases, which begins at an early stage. Elastography is a new ultrasonic technique that characterizes the conditions of lesions in greater detail than B-mode ultrasonography. Elastography is based on two major imaging techniques.
* Corresponding author at: Fukushima Medical University School of Medicine, Department of Otolaryngology, 1 Hikarigaoka, Fukushima 960-1295, Japan. Tel.: +81 24 547 1325; fax: +81 24 548 3011. E-mail address: [email protected] (T. Matsuzuka).
The first method is strain elasticity imaging, also called static elastography. Its implementation requires continuous transducer compression or external mechanical compression. This compression cannot be quantified, and the site of compression cannot be restricted to the specific areas under investigation. The second method is acoustic stress elasticity imaging, or dynamic elastography, including acoustic radiation force impulse (ARFI) imaging, which applies a short-duration acoustic radiation force to the region of interest (ROI) without producing movement of the whole target [1]. This technique requires no external compression and exploits short-duration acoustic radiation forces to generate localized tissue displacements. ARFI imaging can enable qualitative visual and quantitative value measurements [2]. The more elastic a tissue is, the more displacement it undergoes. The displacements result in shear-wave propagation away from the region of excitation and are tracked by using ultrasonic correlation-based methods. By measuring the time to peak displacement at each lateral location, a quantitative implementation named virtual touch
http://dx.doi.org/10.1016/j.anl.2014.08.021 0385-8146/ß 2014 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021
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quantification (VTQ) can calculate the shear wave velocity (SWV) within the tissue. VTQ gives an objective numerical evaluation of the tissue stiffness from 0.8 to 8.4 m/s [3]. Virtual touch imaging quantification (VTIQ) is a new form of two-dimensional shear wave imaging and displays a color-coded image using up to 256 spatially distributed ARFI push pulses and detection pulse sequences that can measure localized SWV from 0.5 to 10 m/s in multiple locations. At present, few clinical results using VTQ and VTIQ have been reported, especially with regard to head and neck lesions. In this study, the VTQ and VTIQ values of normal salivary glands as well as head and neck tumors were measured to evaluate normal salivary gland stiffness and compare the diagnostic performance of VTQ and VTIQ for head and neck tumor. 2. Materials The study was approved by the Institutional Review Board and Ethics Committee of Fukushima Medical University. From March 2013 to November 2013, a total of 38 patients (men: 24, women: 14, age range, 27–85 years; mean age, 65 years) participated in the study. Patients’ clinical records were anonymized and de-identified prior to analysis. Among all 38 of the patients, 15 were follow-up patients after tumor resection and eight were patients with thyroid disease. Seventy-seven salivary glands (parotid gland: 42, submandibular gland: 35), which contained neither mass lesion nor sialoadenitis, were examined and categorized as the normal salivary group (NSG). Fifteen patients had solitary masses (parotid gland: 14, submandiblar gland: 1) in the salivary gland lesions. Four of 15 masses were diagnosed as malignant tumor (acinic cell carcinoma: 2, squamous cell carcinoma: 1, low grade adenoid cystic carcinoma: 1), and were categorized as the malignant tumor group (MTG). The remaining 11 regions were categorized as the benign tumor group (BTG). In total, 92 regions were divided into three groups (NSG, BTG and MTG) and measured with VTQ and VTIQ.
3. Methods 3.1. Virtual touch quantification (VTQ) VTQ measurements were performed with an Acuson S3000 ultrasound system (Siemens Medical Solutions) using a linear array transducer with bandwidth of 4–9 MHz. For VTQ measurement, the patient is required to lie in a position identical to that used for conventional ultrasonography examination. The transducer is gently applied together with a sufficient amount of contact gel. Anatomical location for measurement is defined by region of interest (ROI) placement. Acoustic push pulse is applied adjacent to the ROI with fixed dimensions of 5 mm 5 mm. Tracking beams are then applied adjacent to the acoustic push pulse. Time between generation of the shear wave and the passing of shear wave peak at an adjacent location is utilized to compute the VTQ value in meters per second (m/s, Fig. 1a). Sometimes the VTQ produces nonnumeric results, which are all expressed as X.XX (Fig. 1b). There could be two main reasons to account for such a result: First, the method does not conform to the biomechanical testing standard, and shear waves cannot be generated and propagated in the target. Second, the target is so hard that the results are above the maximum value used by this system [4]. In our study, non-numeric results were considered to be above the measuring range. Each ROI was measured three times in the same region, and the VTQ value was defined as the average of three-time measurements. A nonnumeric VTQ value rate was calculated in each group. 3.2. Virtual touch imaging quantification (VTIQ) For VTIQ measurement, the measuring system, patient position and transducer condition are the same as those for VTQ. A user-defined ROI (maximum size: 25 mm 38 mm) is placed and acoustic push pulses are applied across the ROI. Then stiffness shown by a color-coded two-dimensional shear wave is
Fig. 1. VTQ and VTIQ measurements for 47-year-old female with acinic cell carcinoma of right parotid gland. (a) VTQ value of normal left parotid gland (1.63 m/s, arrowhead) was measured applying adjacent to the ROI with fixed dimensions of 5 mm 5 mm (arrow). (b) VTIQ value of normal left parotid gland (1.67 m/s, arrow) was measured within the user-defined ROI (arrowhead). (c) VTQ value of right parotid tumor, applying adjacent to the ROI (arrow), was expressed as X.XX m/s (arrowhead). This means nonnumeric results were produced. (d) VTIQ values of right parotid tumor (6.51 and 3.80 m/s, arrows).
Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021
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immediately displayed in the ROI on the screen. The VTIQ values within the ROI were quantitatively measured in meters per second (m/s) (Fig 1b and d). As share waves do not propagate in vicious fluid, no signal can be measured e.g. in cysts [5]. In our study, three points were selected in a ROI, and the VTIQ value was defined as the average of three-time measurements. 3.3. Statistical analyses Microsoft Excel 2010 (Microsoft) software was used in the analysis. Mean values (M) and standard deviations (SD) of the VTQ and VTIQ values measured in the central parenchyma of the tumors and normal salivary glands were calculated. The two-tailed t-test with n 2 degrees of freedom was used to compare the mean values of VTQ and VTIQ, Fisher’s exact test was used to compare the non-numeric VTQ value rate, and the level of statistical significance was established at p = 0.05. Receiver operating characteristic curves (ROC) of each VTQ and VTIQ values were calculated to assess their clinical usefulness in identifying malignant tumors, and the area under the receiver operating characteristic curve (AUROC) was evaluated for diagnostic efficacy. 4. Results 92 VTQ values were examined, 84 values were numeric, and ranged from 0.73 to 5.34 m/s (mean: 1.95 m/s, median: 1.90 m/s). Eight of the VTQ values were non-numeric results. When nonnumeric results were considered to be above the measuring range, the median VTQ value was 1.94 m/s. All 92 VTIQ values were numeric, and ranged from 1.01 to 9.03 m/s. The mean and median VTIQ values for all measuring areas were 2.52 1.4SD m/s and 2.04 m/s, respectively. The eighty-four numeric VTQ values were compared with the corresponding 84 VTIQ values. The interclass correlation coefficient between VTQ and VTIQ was 0.62 (y = 0.62x + 1.1, R2 = 0.16, Fig. 2). The VTIQ values corresponding to the 8 non-numeric VTQ values ranged from 4.63 to 9.03 m/s (mean: 6.06 m/s, median: 5.85 m/s). 4.1. VTQ and VTIQ values in normal salivary group (NSG) The VTQ values of all 77 normal salivary glands (parotid gland: 42, submandibular gland: 35) were numeric, and the mean VTQ value was 1.92 0.66 m/s (ranging from 0.73 to 5.34). The mean VTQ
Fig. 3. VTQ value and VTIQ value in normal parotid gland and submandibular gland. (a) Mean VTQ value of normal parotid glands and submandibular glands were 1.98 m/s and 1.86 m/s, respectively. (b) Mean VTIQ value of normal parotid glands and submandibular glands were 2.13 m/s and 1.95 m/s respectively.
values of the normal parotid glands and submandibular glands were 1.98 0.73 (ranging from 0.73 to 5.34) and 1.86 0.37 m/s (ranging from 1.27 to 2.98), respectively, showing no statistical difference. The VTIQ values ranged from 1.00 to 5.56 m/s, and the mean VTIQ value was 2.05 0.61SD m/s. The mean VTIQ values of the normal parotid glands and submandibular glands were 2.13 0.75 (ranging from 1.00 to 5.56) and 1.95 0.35 m/s (ranging from 1.31 to 2.98), respectively, showing no statistical difference. The mean values between VTQ and VTIQ for either the normal parotid glands or submandibular glands showed no statistical difference (Fig. 3). 4.2. VTQ and VTIQ values in benign tumor group (BTG) Four of the 11 VTQ values were non-numeric, and the remaining seven values ranged from 1.25 to 3.05 m/s. When non-numeric results were considered to be above the measuring range, the median VTQ value was 2.63 m/s. The VTIQ values ranged from 1.85 to 6.86 m/s, and the mean VTIQ value was 4.24 1.75SD m/s (median 4.42 m/s). There were no statistical significance of VTQ and VTIQ values between pleomorphic adenoma and Warthin’s tumor (Table 1). 4.3. VTQ and VTIQ values in malignant tumor group (MTG) All four of the VTQ values were non-numeric. The VTIQ values ranged from 4.83 to 9.03 m/s, with a mean value of 6.52 1.94SD m/s (Table 2).
Table 1 Demographics of benign tumor cases.
Fig. 2. The interclass correlation coefficient between VTQ and VTIQ. The interclass correlation coefficient between VTQ and VTIQ values was 0.62 (y = 0.62x + 1.1, R2 = 0.16).
Lesion
Pathological diagnosis
VTQ (m/s)
VTIQ (m/s)
Parotid Parotid Parotid Parotid Parotid Parotid Parotid Parotid Parotid Parotid Submandiblar
Basal cell adenoma Pleomorphic adenoma Pleomorphic adenoma Pleomorphic adenoma Pleomorphic adenoma Pleomorphic adenoma Pleomorphic adenoma Warthin’s tumor Warthin’s tumor Warthin’s tumor Pleomorphic adenoma
X.XX X.XX X.XX 3.05 2.63 2.56 1.25 X.XX 2.18 2.04 2.04
4.63 6.05 5.68 2.07 2.89 6.86 1.85 6.02 3.50 2.69 4.42
X.XX: non-numeric result was produced.
Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021
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4 Table 2 Demographics of malignant tumor cases. Lesion
Pathological diagnosis
VTQ (m/s)
VTIQ (m/s)
Parotid Parotid Parotid Parotid
Squamous cell ca Adenoid-cystic ca Acinic cell ca Acinic cell ca
X.XX X.XX X.XX X.XX
4.83 9.03 7.06 5.16
X.XX, non-numeric result was produced.
4.4. Comparison of VTQ in three groups The non-numeric VTQ value rates in the NSG, BTG and MTG were 0% (0/77), 36.4% (4/11) and 100% (4/4), respectively, and, significant differences were observed (NSG vs BTG: p < 0.001, NSG vs MTG: p < 0.001, Fig. 4a). ROC evaluation showed that VTQ had good discriminative power in relation to histopathological diagnosis, and was highly useful in distinguishing malignant tumors from benign tumors and normal salivary glands in terms of the AUROC (97.9%). In our study, detection of malignant tumors was optimum at a cutoff point of X.XX m/s (sensitivity: 100%, specificity: 95.7%, Fig. 5a). In dividing malignant tumors from benign tumors, area under the curve of VTQ value was 81.8%, when a cutoff value of 4.83 m/s was applied, the sensitivity and specificity were 100% and 63.6%, respectively (Fig. 5b). 4.5. Comparison of VTIQ value in three groups The mean VTIQ values in the NSG, BTG and MTG were 2.05, 4.24 and 6.52 m/s, respectively. Significant differences were observed among the groups (NSG vs BTG: p < 0.001, NSG vs MTG: p < 0.001, BTG vs MTG: p < 0.05, Fig. 4b). ROC evaluation showed that VTIQ also had good discriminative power in relation to histopathological diagnosis, and was highly useful in distinguishing malignant tumors from benign tumors and normal salivary glands in terms of the AUROC (97.1%). In our study, detection of malignant tumors from benign tumors and normal salivary glands was optimum at a cutoff point of 4.83 m/s (sensitivity: 100%, specificity: 94.3%, Fig. 5a). In dividing malignant tumors from benign tumors, area under the curve of VTIQ value was 81.8%, when a cutoff value of 4.83 m/s was applied, the
Fig. 5. Receiver-operator characteristic curves comparing the VTQ and VTIQ value: in dividing malignant tumors from benign tumors and normal salivary glands (a), and in dividing malignant tumors from benign tumors (b). (a) In dividing malignant tumors from benign tumors, and normal salivary glands, area under the curve of VTQ value was 97.9%, when a cutoff value of X.XX m/s was applied, the sensitivity and specificity were 100% and 95.7%, respectively. Area under the curve of VTIQ value was 95.7%, when a cutoff value of 4.83 m/s was applied, the sensitivity and specificity were 100% and 94.3%, respectively. (b) In dividing malignant tumors from benign tumors, area under the curve of VTQ and VTIQ value was 81.8%; when a cutoff value of X.XX m/s (VTQ) or 4.83 m/s (VTIQ) was applied, the sensitivity and specificity were 100% and 63.6%, respectively (Fig. 5b). TPF, true positive fraction; FPF, false positive fraction.
sensitivity and specificity were 100% and 63.6%, respectively (Fig. 5b). 5. Discussion In the preoperative assessment of salivary gland tumor, fine needle aspiration cytology (FNAC) and imaging are commonly used. The sensitivity and specificity of FNAC were reported to be 86% and 100%, respectively [6]. Hypocellular parotid tumors which had thinner capsules and could be vulnerable to operative rupture, especially pleomorphic adenoma, which is a common benign tumor, infrequently undergoes malignant transformation [7]. Regarding indeterminate tumors, surgical excision of the nodule remains the recommended treatment, and an examination that is more sensitive than FNAC may be necessary for preoperative assessment.
Fig. 4. VTQ value and VTIQ value among three groups. (a) The non-numeric rate of VTQ value in NSG, BTG and MTG were 0% (0/77), 36.4% (4/11) and 100% (4/4), respectively. Significant differences in the non-numeric rate of VTQ value were observed (NSG vs BTG: p < 0.001, NSG vs MTG: p < 0.001). (b) The mean VTIQ values in NSG, BTG and MTG were 2.05 m/s, 4.24 m/s and 6.52 m/s, respectively. Significant differences of the mean VTIQ values were observed in three groups (NSG vs BTG: p < 0.001, NSG vs MTG: p < 0.001, BTG vs MTG: p < 0.05).
Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021
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VTQ and VTIQ technologies are classified as ARFI imaging, which uses acoustic radiation force to generate images of the mechanical properties of soft tissue. Acoustic radiation force is a phenomenon associated with the propagation of acoustic waves in an attenuating medium. Attenuation includes absorption of the acoustic wave in soft tissues. With increasing acoustic frequencies, the motion of the tissue becomes out of phase with the acoustic wave, and energy is deposited into the tissue. This energy results in a momentum transfer in the direction of wave propagation and tissue heating. The momentum transfer generates a force that causes displacement of the tissue. This interaction of sound with the tissue can be used to derive additional information about the tissue, beyond what is normally provided in an ultrasonic image [3]. VTQ is a quantitative ARFI imaging that provides single point shear wave speed measurements. VTQ in normal tissue has been performed; some reports described the mean VTQ values of breast tissue (3.33 m/s) [8], liver (1.59 and 1.56 m/s), pancreas (1.40 m/s), spleen (2.44 m/s) and kidney (2.24 m/s) [9,10]. In our study, the mean VTQ value of the normal submandibular glands was 1.86 0.37SD m/s, which is similar to that reported in a Romanian study (1.82 0.41SD m/s) [11]. VTQ values of abnormal lesions provide information for evaluating patients’ conditions and detecting malignant tumors. There is a significant positive correlation between median VTQ value and severity of liver fibrosis in patients with nonalcoholic fatty liver disease [12]. Regarding the detection of malignant tumors, Zhang reported that the mean VTQ value between benign and malignant thyroid tumors was statistically different (p < 0.001), and the cutoff point for malignancy was 2.87 m/s [13]. Wojcinski et al. reported that the mean VTQ value between benign and malignant breast tumor was statistically different (p < 0.001) and the cutoff point for malignancy was set to X.XX m/s [14]. The range of VTQ values is estimated to be between 0.8 and 8.4 m/s, and VTQ values beyond this range are displayed as X.XX m/s, excluding possible influencing factors such as patient’s respiration and operator’s inappropriate gesture, the value of X.XX m/s is allocated to be less than 0.8 m/s or more than 8.4 m/s [15]. Regarding evaluation of parotid gland condition, Badea et al. reported that the mean VTQ value of radiation submaxillitis was statistically higher than that of normal glands [11]. As for detection of parotid gland tumor, Mansour et al. reported that mean VTQ value of pleomorphic adenoma is higher than that of Warthin’s tumor [16]. In their report, two of the four VTQ values for malignant tumor were non-numeric, and there was no difference in VTQ values between the benign and two malignant tumors with numeric results. In our study, eight of the VTQ values were nonnumeric. The VTIQ values corresponding to the eight non-numeric VTQ values ranged from 4.63 to 9.03 m/s (mean: 6.06 m/s, median: 5.85 m/s), and all eight non-numeric VTQ results in the BTG and MTG were surmised to exceed the upper limit of possible measurement. We assume stiffness of some salivary gland tumors was so hard that the results are above the maximum value used by VTQ system. All four VTQ values in the MTG were surmised to exceed the upper limit of possible measurement, and the cutoff point for malignancy was estimated as X.XX m/s with high sensitivity (100%). VTIQ displays color-coded two-dimensional shear wave imaging using up to 256 spatially distributed ARFI push pulse sequences that can measure VTIQ values in multiple locations within the ROI. There have been two clinical reports about VTIQ values: Golatta et al. described the mean VTIQ values of normal breast tissue (3.23 m/s) and fatty tissue (2.50 m/s) [17], and Tozaki et al. described the mean VTIQ values of benign breast tumor (2.27 m/s) and malignant tumor (6.69 m/s), with an estimated cutoff VTIQ
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value for malignant tumors of 4.41 m/s [3]. In our study, all VTIQ values were numeric, the VITQ value range, which was estimated from 0.5 to 10 m/s, was suitable for quantitatively measuring head and neck lesions, and the cutoff point for malignancy was estimated to be 4.83 m/s with high sensitivity (100%). These findings suggest that there is a correlation between VTQ and VTIQ values. The VTQ and VTIQ values for normal salivary glands were 1.92 and 2.06 m/s, respectively, and there were no statistical differences regarding each mean value between normal parotid glands and normal submandibular glands. However, the VTQ values for malignant head and neck tumor were non-numeric, whereas the VTIQ values were numeric. Although the series of this material was small and exploratory validation trial, the optimum VTQ and VTIQ cutoff values to detect malignant tumors were X.XX and 4.83 m/s, respectively. Both VTQ and VTIQ had sensitive preoperative diagnostic value for the identification of malignant tumor in head and neck lesions. VTQ and VTIQ values could be applied for the preoperative diagnosis in salivary gland lesions. A further large-scale study to validate our results and establish the cutoff value to minimize the false omission rate is warranted. 6. Conclusions The VTQ and VTIQ values were correlative for the salivary glands, and the stiffness was similar between the normal parotid glands and submandibular glands, determined through the VTQ and VTIQ values. Both VTQ and VTIQ have sensitive preoperative diagnostic value for the identification of malignant tumor in salivary gland lesions. These methods of quantification could be utilized to evaluate salivary gland and tumor stiffness. Financial support None. Conflict of interest The authors declare that they have no conflicts of interest. References [1] Nightingale K, Soo MS, Nightingale R, Trahey G. Acoustic radiation force impulse imaging: in vivo demonstration of clinical feasibility. Ultrasound Med Biol 2002;28:227–35. [2] Ophir J, Cespedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging 1991;13:111–34. [3] Tozaki M, Saito M, Benson J, Fan L, Isobe S. Shear wave velocity measurements for differential diagnosis of solid breast masses: a comparison between virtual touch quantification and virtual touch IQ. Ultrasound Med Biol 2013;39:2233–45. [4] Bai M, Du L, Gu J, Li F, Jia X. Virtual touch tissue quantification using acoustic radiation force impulse technology: initial clinical experience with solid breast masses. J Ultrasound Med 2012;31:289–94. [5] Athanasiou A, Tardivon A, Tanter M, Sigal-Zafrani B, Bercoff J, Deffieux T, et al. Breast lesions: quantitative elastography with supersonic shear imaging – preliminary results. Radiology 2010;256:297–303. [6] Tryggvason G, Gailey MP, Hulstein SL, Karnell LH, Hoffman HT, Funk GF, et al. Accuracy of fine-needle aspiration and imaging in the preoperative workup of salivary gland mass lesions treated surgically. Laryngoscope 2013;123:158–63. [7] Kato H, Kanematsu M, Mizuta K, Ito Y, Hirose Y. Carcinoma ex pleomorphic adenoma of the parotid gland: radiologic–pathologic correlation with MR imaging including diffusion-weighted imaging. Am J Neuroradiol 2008;29:865–7. [8] Wojcinski S, Brandhorst K, Sadigh G, Hillemanns P, Degenhardt F. Acoustic radiation force impulse imaging with virtual touch tissue quantification: measurements of normal breast tissue and dependence on the degree of pre-compression. Ultrasound Med Biol 2013;39:2226–32. [9] Gallotti A, D’Onofrio M, Pozzi Mucelli R. Acoustic radiation force impulse (ARFI) technique in ultrasound with virtual touch tissue quantification of the upper abdomen. Radiol Med 2010;115:889–97. [10] D’Onofrio M, Gallotti A, Pozzi Mucelli R. Virtual touch tissue quantification: measurement repeatability and normal values in the healthy liver. AJR Am J Roentgenol 2010;195:132–6.
Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021
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shear wave velocity of malignant and benign breast masses. Int J Womens Health 2013;5:619–27. [15] Meng W, Zhang G, Wu C, Wu G, Song Y, Lu Z. Preliminary results of acoustic radiation force impulse (ARFI) ultrasound imaging of breast lesions. Ultrasound Med Biol 2011;37:1436–43. [16] Mansour N, Stock KF, Chaker A, Bas M, Knopf A. Evaluation of parotid gland lesions with standard ultrasound, color duplex sonography, sonoelastography, and acoustic radiation force impulse imaging – a pilot study. Ultraschall Med 2012;33:283–8. [17] Golatta M, Schweitzer-Martin M, Harcos A, Schott S, Junkermann H, Rauch G, et al. Normal breast tissue stiffness measured by a new ultrasound technique: virtual touch tissue imaging quantification (VTIQ). Eur J Radiol 2013;82:e676–9.
Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021
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Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ Takashi Matsuzuka MD, PhD*, Masahiro Suzuki MD, Satoshi Saijo MD, Masakazu Ikeda MD, Takamichi Matsui MD, PhD, Yukio Nomoto MD, PhD, Mika Nomoto MD, PhD, Mitsuyoshi Imaizumi MD, PhD, Yasuhiro Tada MD, PhD, Koichi Omori MD, PhD Department of Otolaryngology, Fukushima Medical University School of Medicine, Japan
A R T I C L E I N F O
A B S T R A C T
Article history: Received 22 June 2014 Accepted 15 August 2014 Available online xxx
Objective: To evaluate normal salivary gland stiffness and compare the diagnostic performance of virtual touch quantification (VTQ) and virtual touch imaging quantification (VTIQ) for head and neck tumor. Methods: A total of 92 measurements were examined, comprising 77 normal salivary glands, 11 benign tumors and four malignant tumors. Examinations were made to evaluate normal salivary gland stiffness and compare the diagnostic performances of new ultrasonic techniques regarding head and neck tumor. Results: The mean values of VTQ and VTIQ for the normal salivary group (NSG) were 1.92 and 2.06 m/s, respectively. The VTQ and VTIQ values were correlative, and there were no statistical differences in each mean value between the normal parotid glands and submandibular glands. For the benign tumor group (BTG), four of the 11 values were non-numeric and were considered above the measurable range. The mean VTIQ value for the BTG was 4.24 m/s. For the malignant tumor group (MTG), all four VTQ values were non-numeric. The mean VTIQ value for the MTG was 6.52 m/s. For the mean VTIQ values, significant differences were observed among the three groups. The optimum VTQ cutoff value to detect malignant tumors was above the measurable range, and that of VTIQ was 4.83 m/s. Conclusion: The VTQ and VTIQ values were correlative for the salivary glands, and the stiffnesses of normal parotid glands were almost same as those of submandibular glands. VTQ and VTIQ values could be applied for the preoperative diagnosis in salivary gland lesions. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Normal salivary gland Head and neck tumor Salivary gland tumor Acoustic radiation force impulse (ARFI) Virtual touch tissue quantification (VTQ) Virtual touch tissue imaging quantification (VTIQ)
1. Introduction In salivary gland tumor, although most head and neck cancer is diagnosed pathologically with squamous cell carcinoma, there are various histopathological types, of which squamous cell carcinoma is rare. One of the most serious problems regarding salivary gland tumor is that many are difficult to identify as either benign or malignant before treatment. Due to the density of the cancer cells and blood vessels, the stiffness of the cancer tissue increases, which begins at an early stage. Elastography is a new ultrasonic technique that characterizes the conditions of lesions in greater detail than B-mode ultrasonography. Elastography is based on two major imaging techniques.
* Corresponding author at: Fukushima Medical University School of Medicine, Department of Otolaryngology, 1 Hikarigaoka, Fukushima 960-1295, Japan. Tel.: +81 24 547 1325; fax: +81 24 548 3011. E-mail address: [email protected] (T. Matsuzuka).
The first method is strain elasticity imaging, also called static elastography. Its implementation requires continuous transducer compression or external mechanical compression. This compression cannot be quantified, and the site of compression cannot be restricted to the specific areas under investigation. The second method is acoustic stress elasticity imaging, or dynamic elastography, including acoustic radiation force impulse (ARFI) imaging, which applies a short-duration acoustic radiation force to the region of interest (ROI) without producing movement of the whole target [1]. This technique requires no external compression and exploits short-duration acoustic radiation forces to generate localized tissue displacements. ARFI imaging can enable qualitative visual and quantitative value measurements [2]. The more elastic a tissue is, the more displacement it undergoes. The displacements result in shear-wave propagation away from the region of excitation and are tracked by using ultrasonic correlation-based methods. By measuring the time to peak displacement at each lateral location, a quantitative implementation named virtual touch
http://dx.doi.org/10.1016/j.anl.2014.08.021 0385-8146/ß 2014 Elsevier Ireland Ltd. All rights reserved.
Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021
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quantification (VTQ) can calculate the shear wave velocity (SWV) within the tissue. VTQ gives an objective numerical evaluation of the tissue stiffness from 0.8 to 8.4 m/s [3]. Virtual touch imaging quantification (VTIQ) is a new form of two-dimensional shear wave imaging and displays a color-coded image using up to 256 spatially distributed ARFI push pulses and detection pulse sequences that can measure localized SWV from 0.5 to 10 m/s in multiple locations. At present, few clinical results using VTQ and VTIQ have been reported, especially with regard to head and neck lesions. In this study, the VTQ and VTIQ values of normal salivary glands as well as head and neck tumors were measured to evaluate normal salivary gland stiffness and compare the diagnostic performance of VTQ and VTIQ for head and neck tumor. 2. Materials The study was approved by the Institutional Review Board and Ethics Committee of Fukushima Medical University. From March 2013 to November 2013, a total of 38 patients (men: 24, women: 14, age range, 27–85 years; mean age, 65 years) participated in the study. Patients’ clinical records were anonymized and de-identified prior to analysis. Among all 38 of the patients, 15 were follow-up patients after tumor resection and eight were patients with thyroid disease. Seventy-seven salivary glands (parotid gland: 42, submandibular gland: 35), which contained neither mass lesion nor sialoadenitis, were examined and categorized as the normal salivary group (NSG). Fifteen patients had solitary masses (parotid gland: 14, submandiblar gland: 1) in the salivary gland lesions. Four of 15 masses were diagnosed as malignant tumor (acinic cell carcinoma: 2, squamous cell carcinoma: 1, low grade adenoid cystic carcinoma: 1), and were categorized as the malignant tumor group (MTG). The remaining 11 regions were categorized as the benign tumor group (BTG). In total, 92 regions were divided into three groups (NSG, BTG and MTG) and measured with VTQ and VTIQ.
3. Methods 3.1. Virtual touch quantification (VTQ) VTQ measurements were performed with an Acuson S3000 ultrasound system (Siemens Medical Solutions) using a linear array transducer with bandwidth of 4–9 MHz. For VTQ measurement, the patient is required to lie in a position identical to that used for conventional ultrasonography examination. The transducer is gently applied together with a sufficient amount of contact gel. Anatomical location for measurement is defined by region of interest (ROI) placement. Acoustic push pulse is applied adjacent to the ROI with fixed dimensions of 5 mm 5 mm. Tracking beams are then applied adjacent to the acoustic push pulse. Time between generation of the shear wave and the passing of shear wave peak at an adjacent location is utilized to compute the VTQ value in meters per second (m/s, Fig. 1a). Sometimes the VTQ produces nonnumeric results, which are all expressed as X.XX (Fig. 1b). There could be two main reasons to account for such a result: First, the method does not conform to the biomechanical testing standard, and shear waves cannot be generated and propagated in the target. Second, the target is so hard that the results are above the maximum value used by this system [4]. In our study, non-numeric results were considered to be above the measuring range. Each ROI was measured three times in the same region, and the VTQ value was defined as the average of three-time measurements. A nonnumeric VTQ value rate was calculated in each group. 3.2. Virtual touch imaging quantification (VTIQ) For VTIQ measurement, the measuring system, patient position and transducer condition are the same as those for VTQ. A user-defined ROI (maximum size: 25 mm 38 mm) is placed and acoustic push pulses are applied across the ROI. Then stiffness shown by a color-coded two-dimensional shear wave is
Fig. 1. VTQ and VTIQ measurements for 47-year-old female with acinic cell carcinoma of right parotid gland. (a) VTQ value of normal left parotid gland (1.63 m/s, arrowhead) was measured applying adjacent to the ROI with fixed dimensions of 5 mm 5 mm (arrow). (b) VTIQ value of normal left parotid gland (1.67 m/s, arrow) was measured within the user-defined ROI (arrowhead). (c) VTQ value of right parotid tumor, applying adjacent to the ROI (arrow), was expressed as X.XX m/s (arrowhead). This means nonnumeric results were produced. (d) VTIQ values of right parotid tumor (6.51 and 3.80 m/s, arrows).
Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021
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immediately displayed in the ROI on the screen. The VTIQ values within the ROI were quantitatively measured in meters per second (m/s) (Fig 1b and d). As share waves do not propagate in vicious fluid, no signal can be measured e.g. in cysts [5]. In our study, three points were selected in a ROI, and the VTIQ value was defined as the average of three-time measurements. 3.3. Statistical analyses Microsoft Excel 2010 (Microsoft) software was used in the analysis. Mean values (M) and standard deviations (SD) of the VTQ and VTIQ values measured in the central parenchyma of the tumors and normal salivary glands were calculated. The two-tailed t-test with n 2 degrees of freedom was used to compare the mean values of VTQ and VTIQ, Fisher’s exact test was used to compare the non-numeric VTQ value rate, and the level of statistical significance was established at p = 0.05. Receiver operating characteristic curves (ROC) of each VTQ and VTIQ values were calculated to assess their clinical usefulness in identifying malignant tumors, and the area under the receiver operating characteristic curve (AUROC) was evaluated for diagnostic efficacy. 4. Results 92 VTQ values were examined, 84 values were numeric, and ranged from 0.73 to 5.34 m/s (mean: 1.95 m/s, median: 1.90 m/s). Eight of the VTQ values were non-numeric results. When nonnumeric results were considered to be above the measuring range, the median VTQ value was 1.94 m/s. All 92 VTIQ values were numeric, and ranged from 1.01 to 9.03 m/s. The mean and median VTIQ values for all measuring areas were 2.52 1.4SD m/s and 2.04 m/s, respectively. The eighty-four numeric VTQ values were compared with the corresponding 84 VTIQ values. The interclass correlation coefficient between VTQ and VTIQ was 0.62 (y = 0.62x + 1.1, R2 = 0.16, Fig. 2). The VTIQ values corresponding to the 8 non-numeric VTQ values ranged from 4.63 to 9.03 m/s (mean: 6.06 m/s, median: 5.85 m/s). 4.1. VTQ and VTIQ values in normal salivary group (NSG) The VTQ values of all 77 normal salivary glands (parotid gland: 42, submandibular gland: 35) were numeric, and the mean VTQ value was 1.92 0.66 m/s (ranging from 0.73 to 5.34). The mean VTQ
Fig. 3. VTQ value and VTIQ value in normal parotid gland and submandibular gland. (a) Mean VTQ value of normal parotid glands and submandibular glands were 1.98 m/s and 1.86 m/s, respectively. (b) Mean VTIQ value of normal parotid glands and submandibular glands were 2.13 m/s and 1.95 m/s respectively.
values of the normal parotid glands and submandibular glands were 1.98 0.73 (ranging from 0.73 to 5.34) and 1.86 0.37 m/s (ranging from 1.27 to 2.98), respectively, showing no statistical difference. The VTIQ values ranged from 1.00 to 5.56 m/s, and the mean VTIQ value was 2.05 0.61SD m/s. The mean VTIQ values of the normal parotid glands and submandibular glands were 2.13 0.75 (ranging from 1.00 to 5.56) and 1.95 0.35 m/s (ranging from 1.31 to 2.98), respectively, showing no statistical difference. The mean values between VTQ and VTIQ for either the normal parotid glands or submandibular glands showed no statistical difference (Fig. 3). 4.2. VTQ and VTIQ values in benign tumor group (BTG) Four of the 11 VTQ values were non-numeric, and the remaining seven values ranged from 1.25 to 3.05 m/s. When non-numeric results were considered to be above the measuring range, the median VTQ value was 2.63 m/s. The VTIQ values ranged from 1.85 to 6.86 m/s, and the mean VTIQ value was 4.24 1.75SD m/s (median 4.42 m/s). There were no statistical significance of VTQ and VTIQ values between pleomorphic adenoma and Warthin’s tumor (Table 1). 4.3. VTQ and VTIQ values in malignant tumor group (MTG) All four of the VTQ values were non-numeric. The VTIQ values ranged from 4.83 to 9.03 m/s, with a mean value of 6.52 1.94SD m/s (Table 2).
Table 1 Demographics of benign tumor cases.
Fig. 2. The interclass correlation coefficient between VTQ and VTIQ. The interclass correlation coefficient between VTQ and VTIQ values was 0.62 (y = 0.62x + 1.1, R2 = 0.16).
Lesion
Pathological diagnosis
VTQ (m/s)
VTIQ (m/s)
Parotid Parotid Parotid Parotid Parotid Parotid Parotid Parotid Parotid Parotid Submandiblar
Basal cell adenoma Pleomorphic adenoma Pleomorphic adenoma Pleomorphic adenoma Pleomorphic adenoma Pleomorphic adenoma Pleomorphic adenoma Warthin’s tumor Warthin’s tumor Warthin’s tumor Pleomorphic adenoma
X.XX X.XX X.XX 3.05 2.63 2.56 1.25 X.XX 2.18 2.04 2.04
4.63 6.05 5.68 2.07 2.89 6.86 1.85 6.02 3.50 2.69 4.42
X.XX: non-numeric result was produced.
Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021
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4 Table 2 Demographics of malignant tumor cases. Lesion
Pathological diagnosis
VTQ (m/s)
VTIQ (m/s)
Parotid Parotid Parotid Parotid
Squamous cell ca Adenoid-cystic ca Acinic cell ca Acinic cell ca
X.XX X.XX X.XX X.XX
4.83 9.03 7.06 5.16
X.XX, non-numeric result was produced.
4.4. Comparison of VTQ in three groups The non-numeric VTQ value rates in the NSG, BTG and MTG were 0% (0/77), 36.4% (4/11) and 100% (4/4), respectively, and, significant differences were observed (NSG vs BTG: p < 0.001, NSG vs MTG: p < 0.001, Fig. 4a). ROC evaluation showed that VTQ had good discriminative power in relation to histopathological diagnosis, and was highly useful in distinguishing malignant tumors from benign tumors and normal salivary glands in terms of the AUROC (97.9%). In our study, detection of malignant tumors was optimum at a cutoff point of X.XX m/s (sensitivity: 100%, specificity: 95.7%, Fig. 5a). In dividing malignant tumors from benign tumors, area under the curve of VTQ value was 81.8%, when a cutoff value of 4.83 m/s was applied, the sensitivity and specificity were 100% and 63.6%, respectively (Fig. 5b). 4.5. Comparison of VTIQ value in three groups The mean VTIQ values in the NSG, BTG and MTG were 2.05, 4.24 and 6.52 m/s, respectively. Significant differences were observed among the groups (NSG vs BTG: p < 0.001, NSG vs MTG: p < 0.001, BTG vs MTG: p < 0.05, Fig. 4b). ROC evaluation showed that VTIQ also had good discriminative power in relation to histopathological diagnosis, and was highly useful in distinguishing malignant tumors from benign tumors and normal salivary glands in terms of the AUROC (97.1%). In our study, detection of malignant tumors from benign tumors and normal salivary glands was optimum at a cutoff point of 4.83 m/s (sensitivity: 100%, specificity: 94.3%, Fig. 5a). In dividing malignant tumors from benign tumors, area under the curve of VTIQ value was 81.8%, when a cutoff value of 4.83 m/s was applied, the
Fig. 5. Receiver-operator characteristic curves comparing the VTQ and VTIQ value: in dividing malignant tumors from benign tumors and normal salivary glands (a), and in dividing malignant tumors from benign tumors (b). (a) In dividing malignant tumors from benign tumors, and normal salivary glands, area under the curve of VTQ value was 97.9%, when a cutoff value of X.XX m/s was applied, the sensitivity and specificity were 100% and 95.7%, respectively. Area under the curve of VTIQ value was 95.7%, when a cutoff value of 4.83 m/s was applied, the sensitivity and specificity were 100% and 94.3%, respectively. (b) In dividing malignant tumors from benign tumors, area under the curve of VTQ and VTIQ value was 81.8%; when a cutoff value of X.XX m/s (VTQ) or 4.83 m/s (VTIQ) was applied, the sensitivity and specificity were 100% and 63.6%, respectively (Fig. 5b). TPF, true positive fraction; FPF, false positive fraction.
sensitivity and specificity were 100% and 63.6%, respectively (Fig. 5b). 5. Discussion In the preoperative assessment of salivary gland tumor, fine needle aspiration cytology (FNAC) and imaging are commonly used. The sensitivity and specificity of FNAC were reported to be 86% and 100%, respectively [6]. Hypocellular parotid tumors which had thinner capsules and could be vulnerable to operative rupture, especially pleomorphic adenoma, which is a common benign tumor, infrequently undergoes malignant transformation [7]. Regarding indeterminate tumors, surgical excision of the nodule remains the recommended treatment, and an examination that is more sensitive than FNAC may be necessary for preoperative assessment.
Fig. 4. VTQ value and VTIQ value among three groups. (a) The non-numeric rate of VTQ value in NSG, BTG and MTG were 0% (0/77), 36.4% (4/11) and 100% (4/4), respectively. Significant differences in the non-numeric rate of VTQ value were observed (NSG vs BTG: p < 0.001, NSG vs MTG: p < 0.001). (b) The mean VTIQ values in NSG, BTG and MTG were 2.05 m/s, 4.24 m/s and 6.52 m/s, respectively. Significant differences of the mean VTIQ values were observed in three groups (NSG vs BTG: p < 0.001, NSG vs MTG: p < 0.001, BTG vs MTG: p < 0.05).
Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021
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VTQ and VTIQ technologies are classified as ARFI imaging, which uses acoustic radiation force to generate images of the mechanical properties of soft tissue. Acoustic radiation force is a phenomenon associated with the propagation of acoustic waves in an attenuating medium. Attenuation includes absorption of the acoustic wave in soft tissues. With increasing acoustic frequencies, the motion of the tissue becomes out of phase with the acoustic wave, and energy is deposited into the tissue. This energy results in a momentum transfer in the direction of wave propagation and tissue heating. The momentum transfer generates a force that causes displacement of the tissue. This interaction of sound with the tissue can be used to derive additional information about the tissue, beyond what is normally provided in an ultrasonic image [3]. VTQ is a quantitative ARFI imaging that provides single point shear wave speed measurements. VTQ in normal tissue has been performed; some reports described the mean VTQ values of breast tissue (3.33 m/s) [8], liver (1.59 and 1.56 m/s), pancreas (1.40 m/s), spleen (2.44 m/s) and kidney (2.24 m/s) [9,10]. In our study, the mean VTQ value of the normal submandibular glands was 1.86 0.37SD m/s, which is similar to that reported in a Romanian study (1.82 0.41SD m/s) [11]. VTQ values of abnormal lesions provide information for evaluating patients’ conditions and detecting malignant tumors. There is a significant positive correlation between median VTQ value and severity of liver fibrosis in patients with nonalcoholic fatty liver disease [12]. Regarding the detection of malignant tumors, Zhang reported that the mean VTQ value between benign and malignant thyroid tumors was statistically different (p < 0.001), and the cutoff point for malignancy was 2.87 m/s [13]. Wojcinski et al. reported that the mean VTQ value between benign and malignant breast tumor was statistically different (p < 0.001) and the cutoff point for malignancy was set to X.XX m/s [14]. The range of VTQ values is estimated to be between 0.8 and 8.4 m/s, and VTQ values beyond this range are displayed as X.XX m/s, excluding possible influencing factors such as patient’s respiration and operator’s inappropriate gesture, the value of X.XX m/s is allocated to be less than 0.8 m/s or more than 8.4 m/s [15]. Regarding evaluation of parotid gland condition, Badea et al. reported that the mean VTQ value of radiation submaxillitis was statistically higher than that of normal glands [11]. As for detection of parotid gland tumor, Mansour et al. reported that mean VTQ value of pleomorphic adenoma is higher than that of Warthin’s tumor [16]. In their report, two of the four VTQ values for malignant tumor were non-numeric, and there was no difference in VTQ values between the benign and two malignant tumors with numeric results. In our study, eight of the VTQ values were nonnumeric. The VTIQ values corresponding to the eight non-numeric VTQ values ranged from 4.63 to 9.03 m/s (mean: 6.06 m/s, median: 5.85 m/s), and all eight non-numeric VTQ results in the BTG and MTG were surmised to exceed the upper limit of possible measurement. We assume stiffness of some salivary gland tumors was so hard that the results are above the maximum value used by VTQ system. All four VTQ values in the MTG were surmised to exceed the upper limit of possible measurement, and the cutoff point for malignancy was estimated as X.XX m/s with high sensitivity (100%). VTIQ displays color-coded two-dimensional shear wave imaging using up to 256 spatially distributed ARFI push pulse sequences that can measure VTIQ values in multiple locations within the ROI. There have been two clinical reports about VTIQ values: Golatta et al. described the mean VTIQ values of normal breast tissue (3.23 m/s) and fatty tissue (2.50 m/s) [17], and Tozaki et al. described the mean VTIQ values of benign breast tumor (2.27 m/s) and malignant tumor (6.69 m/s), with an estimated cutoff VTIQ
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value for malignant tumors of 4.41 m/s [3]. In our study, all VTIQ values were numeric, the VITQ value range, which was estimated from 0.5 to 10 m/s, was suitable for quantitatively measuring head and neck lesions, and the cutoff point for malignancy was estimated to be 4.83 m/s with high sensitivity (100%). These findings suggest that there is a correlation between VTQ and VTIQ values. The VTQ and VTIQ values for normal salivary glands were 1.92 and 2.06 m/s, respectively, and there were no statistical differences regarding each mean value between normal parotid glands and normal submandibular glands. However, the VTQ values for malignant head and neck tumor were non-numeric, whereas the VTIQ values were numeric. Although the series of this material was small and exploratory validation trial, the optimum VTQ and VTIQ cutoff values to detect malignant tumors were X.XX and 4.83 m/s, respectively. Both VTQ and VTIQ had sensitive preoperative diagnostic value for the identification of malignant tumor in head and neck lesions. VTQ and VTIQ values could be applied for the preoperative diagnosis in salivary gland lesions. A further large-scale study to validate our results and establish the cutoff value to minimize the false omission rate is warranted. 6. Conclusions The VTQ and VTIQ values were correlative for the salivary glands, and the stiffness was similar between the normal parotid glands and submandibular glands, determined through the VTQ and VTIQ values. Both VTQ and VTIQ have sensitive preoperative diagnostic value for the identification of malignant tumor in salivary gland lesions. These methods of quantification could be utilized to evaluate salivary gland and tumor stiffness. Financial support None. Conflict of interest The authors declare that they have no conflicts of interest. References [1] Nightingale K, Soo MS, Nightingale R, Trahey G. Acoustic radiation force impulse imaging: in vivo demonstration of clinical feasibility. Ultrasound Med Biol 2002;28:227–35. [2] Ophir J, Cespedes I, Ponnekanti H, Yazdi Y, Li X. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason Imaging 1991;13:111–34. [3] Tozaki M, Saito M, Benson J, Fan L, Isobe S. Shear wave velocity measurements for differential diagnosis of solid breast masses: a comparison between virtual touch quantification and virtual touch IQ. Ultrasound Med Biol 2013;39:2233–45. [4] Bai M, Du L, Gu J, Li F, Jia X. Virtual touch tissue quantification using acoustic radiation force impulse technology: initial clinical experience with solid breast masses. J Ultrasound Med 2012;31:289–94. [5] Athanasiou A, Tardivon A, Tanter M, Sigal-Zafrani B, Bercoff J, Deffieux T, et al. Breast lesions: quantitative elastography with supersonic shear imaging – preliminary results. Radiology 2010;256:297–303. [6] Tryggvason G, Gailey MP, Hulstein SL, Karnell LH, Hoffman HT, Funk GF, et al. Accuracy of fine-needle aspiration and imaging in the preoperative workup of salivary gland mass lesions treated surgically. Laryngoscope 2013;123:158–63. [7] Kato H, Kanematsu M, Mizuta K, Ito Y, Hirose Y. Carcinoma ex pleomorphic adenoma of the parotid gland: radiologic–pathologic correlation with MR imaging including diffusion-weighted imaging. Am J Neuroradiol 2008;29:865–7. [8] Wojcinski S, Brandhorst K, Sadigh G, Hillemanns P, Degenhardt F. Acoustic radiation force impulse imaging with virtual touch tissue quantification: measurements of normal breast tissue and dependence on the degree of pre-compression. Ultrasound Med Biol 2013;39:2226–32. [9] Gallotti A, D’Onofrio M, Pozzi Mucelli R. Acoustic radiation force impulse (ARFI) technique in ultrasound with virtual touch tissue quantification of the upper abdomen. Radiol Med 2010;115:889–97. [10] D’Onofrio M, Gallotti A, Pozzi Mucelli R. Virtual touch tissue quantification: measurement repeatability and normal values in the healthy liver. AJR Am J Roentgenol 2010;195:132–6.
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Please cite this article in press as: Matsuzuka T, et al. Stiffness of salivary gland and tumor measured by new ultrasonic techniques: Virtual touch quantification and IQ. Auris Nasus Larynx (2014), http://dx.doi.org/10.1016/j.anl.2014.08.021