Comparison of Virtual Touch Tissue Quantification and Virtual Touch Tissue Imaging Quantification for diagnosis of solid breast tumors of different sizes

Abstract

BACKGROUND: Acoustic radiation force impulse imaging (ARFI) with Virtual Touch Tissue Quantification (VTQ) or Virtual Touch Tissue Imaging Quantification (VTIQ) measures shear wave velocity (SWV), which is proportional to tissue stiffness, a diagnostic parameter for malignancy.

OBJECTIVE: To compare the performance of VTQ and VTIQ in diagnosing solid breast tumors.

METHODS: Conventional ultrasound, VTQ and VTIQ were used to examine 246 solid breast tumors from 230 patients. Tumors were grouped according to size: <10 mm, 10–20 mm, >20 mm. Pathological diagnoses were via histological examination of biopsies. ROC curves were used to assess diagnostic performance and optimal cut-off points for VTQ and VTIQ.

RESULTS: For all sizes, SWV_VTQ and SWV_VTIQ were higher for malignant versus benign tumors (P < 0.05). SWV_VTQ and SWV_VTIQ were both higher for tumors≥10 mm (P < 0.05). Areas under the ROC curves (diagnostic performance index; 0.860–0.952) did not differ significantly between VTQ and VTIQ. Optimal cut-off values for SWV_VTQ and SWV_VTIQ were higher for tumors≥10 mm.

CONCLUSION: The diagnostic performance of VTQ and VTIQ was moderate to good for solid breast tumors. Although both methods have higher sensitivities in tumors≥10 mm, their overall diagnostic performance was similar for all sizes.

Keywords

Virtual Touch Tissue Quantification Virtual Touch Tissue Imaging Quantification shear wave velocity breast tumor tumor size

1 Introduction

As is the case for most other countries, breast cancer is the most common malignancy in Chinese women. In 2008, China accounted for 12.2% of global cases and 9.6% of related deaths [6]. Early detection and accurate diagnosis are vitally important to guide clinical treatment so that survival rates and quality of life can be improved. Conventional ultrasound and mammography provide much information about breast tumors, such as their shape, margin, boundary, echo intensity, microcalcification and blood flow, while contrast-enhanced ultrasound (CEUS) provides information about blood volume and perfusion of parenchymal tissues [11]. However, they do not allow measurement of tissue stiffness, and in the breast, cancers tend to be stiffer than benign lesions [10 , 30]. Ultrasound elastography is a technique for measuring tissue stiffness. For solid masses in the breast, it is reported to improve the specificity of ultrasound diagnoses [10 , 30]. The latest technical development in tissue elastography is the use of either Virtual Touch Tissue Quantification (VTQ) or Virtual Touch Tissue Imaging Quantification (VTIQ) to allow quantitative measurements of tissue stiffness such as liver tissue, breast lesions, testicular and thyroid diseases [3 , 26] to be ascertained from acoustic radiation force impulse imaging (ARFI). Their performance especially in breast lesions has been thoroughly investigated in recent studies and the results show that both methods can accurately distinguish benign and malignant breast lesions [9, 14]. Since they both quantify tissue stiffness based on the shear wave velocity in the tissue, we set out to investigate which is better.

The size of a tumor can influence diagnosis, so we classified them according to their size and then compared the diagnostic performance of VTQ with that of VTIQ, in terms of the differential diagnosis of solid breast tumors.

2 Materials and methods

2.1 Patients

This study was conducted in accordance with the ethical guidelines of the Helsinki Declaration and approved by the Ethics Committee of the Tenth People’s Hospital of Tongji University. From October 2014 to October 2015, 230 patients (246 breast tumors) were enrolled in our study. The patients were aged from 16 to 84 years old and the mean age was 45.76±14.48 years. The inclusion criteria were as follows: (1) solid breast tumor with cystic areas composing <25%, (2) the minimum diameter of the lesion was >6 mm, (3) the patient had not yet received any treatment for the tumor, (4) pathological diagnosis was obtained via histological examination of a surgical or needle biopsy(s). All breast tumors were categorized into one of three groups according to their size (diameter): <10 mm, 10–20 mm or >20 mm. All included patients who were over 18 years old and gave written informed consent prior to enrollment.

2.2 Examination

Conventional ultrasound and ARFI (VTQ and VTIQ) were performed on the breasts using an ACUSON S3000 ultrasound system (Siemens Medical Solutions, Mountain View, CA, USA), equipped with a linear array transducer with a bandwidth of 4–9 MHz. During the examination, all patients were in the supine position with the breast and axillary fossa fully exposed.

The conventional scan, which could provide size of breast lesions and distinguish cysts from solid breast masses efficiently [19], was carried out first, and the size, shape, margin, internal echo, back echo and color flow of the tumors were recorded from the best images. Next, VTQ mode was used. The region of interest (ROI) was placed in the center of the tumor on the gray scale sonograph. Patients breathing heavily were asked to hold their breath during acquisition. To prevent artifactual stiffness from being recorded, the transducer was maintained in a relatively fixed position and manual pressure on the transducer during image build-up was avoided. Shear wave velocity (SWV) was automatically calculated by the manufacturer-provided software and displayed on the monitor. Subsequently, the ultrasound device was switched to VTIQ mode, which is a new ARFI elastography method with color-coded qualitative and quantitative maps. The color scale varied from blue to red; representing low to high relative SWV values, respectively. SWV was measured within the ROI inside the tumor. The surrounding background varied from blue to blue-green and the tumors were red or yellow for the standard at the end to image after adjusting the velocity range. ROIs were marked within the tumors, avoiding areas of calcification, necrosis and liquefaction (Fig. 1). The SWV_VTQ and SWV_VTIQ for each tumor were measured eight times and averaged for further analysis.

2.3 Imaging evaluation

In order to reduce inter-observer variability, a single consultant specialist with more than 10 years experience in breast examination performed all the measurements. This consultant received ARFI training from the device manufacturer. In cases where the measurements were outside the acceptable range of the VTQ system (0.5–8.4 m/s), the SWV_VTQ was shown as “X.XX m/s” by the software. Because of our exclusion of cysts and tumors with cystic areas exceeding 25%, we took 8.4 m/s for the value of X.XX m/s as previously described by Tang et al. [23]. When the SWV_VTIQ was given as “NA” by the software, the velocity had exceeded the upper limit of the VTIQ system, 10 m/s, and thus “NA” was recorded as 10 m/s.

2.4 Data and statistical analysis

Statistical data were processed and analyzed using SPSS 19.0. The SWV values within the ROI were expressed as the mean±standard deviation (SD). Independent t-tests were used to compare the benign and malignant mean-velocity values. Dunnett’s T3, a type of one-way analysis of variance (ANOVA-1), was used to compare the mean SWV values of the malignant tumors across the three groups. Receiver operating characteristic (ROC) curves were constructed allowing determination of the optimal cut-off points for SWV values and the areas under the curves (AUCs) which were subsequently compared using the z test. Differences were considered statistically significant if P was <0.05.

3 Results

3.1 Pathology results

All breast tumors were cytologically or histologically examined. The results indicated that, out of 246 tumors, 169 (68.7%) were benign and 77 (31.3%) were malignant. The majority of benign tumors were confirmed as fibroadenomas (104, 61.5%), and most of the malignant tumors were invasive ductal carcinomas (58, 75.3%). The histologic findings for the two groups are summarized in Table 1.

3.2 Comparison of mean SWV in benign and malignant tumors of different sizes

The mean SWV_VTQ and SWV_VTIQ values obtained from eight measurements of each lesion are shown in Table 2. Of the 65 breast tumors that were <10 mm in diameter, 49 (75.38%) were benign and 16 (24.62%) were malignant. In this tumor-size group, the mean SWV_VTQ was 2.45±1.06 m/s for benign tumors and 4.49±2.22 m/s for malignant tumors. Mean SWV_VTIQ values for benign and malignant tumors were 2.88±1.00 m/s and 4.32±1.41 m/s, respectively. The 10–20 mm group was the largest of the three, containing 107 tumors; of which, 81 (75.70%) were benign and 26 (24.30%) were malignant. The mean SWV_VTQ and SWV_VTIQ values for benign tumors in this group were 2.93±1.25 m/s and 3.21±1.12 m/s, respectively, and for malignant tumors, they were 7.07±1.80 m/s and 5.63±1.87 m/s. There were 74 tumors >20 mm in diameter; 39 (52.70%) of these were benign and 35 (47.30%) were malignant. For the benign tumors, the mean SWV_VTQ and SWV_VTIQ values were 3.21±1.21 m/s and 3.58±1.01 m/s, respectively, and for malignant cases they were 7.44±1.71 m/s and 6.06±1.46 m/s. Taking these results together, the mean SWV was found to be higher for malignant tumors of all sizes, whether measured by VTQ or by VTIQ (P < 0.05 for all).

3.3 ROC curves for VTQ and VTIQ

Receiver-operating characteristic (ROC) curves plot the true positive rate against the false positive rate for all possible cut-off values of a diagnostic-test parameter; they illustrate the relationship between sensitivity and specificity for ordinal outcomes. The diagnostic performance is represented by the area under the ROC curve (AUC).

Based on the actual (pathological) diagnoses, we constructed ROC curves (Fig. 2) for SWV_VTQ and SWV_VTIQ in each of the three tumor-size groups; the results are shown in Table 3. In tumors <10 mm, the AUC of SWV_VTIQ was 0.871 (95% CI 0.765–0.941), whereas it was a little smaller for SWV_VTQ, at 0.860 (95% CI 0.752–0.934). In contrast, for the two larger tumor groups, AUCs were smaller for SWV_VTIQ: 0.901 (95% CI 0.828–0.950) versus 0.917 (95% CI 0.848–0.962) for tumors of 10–20 mm; and 0.914 (95% CI 0.825–0.966) versus 0.952 (95% CI 0.875–0.988) for those >20 mm. However, z tests indicated that none of these small AUC differences were statistically significant (P > 0.05). Nevertheless, all AUCs were above 0.800 and a value of 0.952 was attained for VTQ in tumors >20 mm. Therefore, the diagnostic performance was of moderate or better, regardless of whether VTQ or VTIQ was used.

3.4 Comparison of mean SWV for malignant tumors of different sizes

We compared the mean SWV values for malignant tumors alone. When tumors were <10 mm, the mean SWV_VTQ was only 4.49±2.22 m/s and the mean SWV_VTIQ was 4.32±1.41 m/s, which were significantly lower than the mean SWV_VTQ and SWV_VTIQ values for tumors in the other two groups (P < 0.05). In contrast, no significant difference existed between these two groups representing the larger tumors, in terms of either SWV_VTQ or SWV_VTIQ (P > 0.05; Table 4).

3.5 Optimal cut-off values for SWV to distinguish benign and malignant solid breast tumors

The basic statistical measures of performance for a diagnostic test are sensitivity and specificity. The optimal cut-off value produced the maximal sum of sensitivity and specificity according to the ROC curve (Table 5). For tumors <10 mm, the respective cut-off values for SWV_VTQ and SWV_VTIQ were found to be 2.94 m/s and 3.78 m/s; this corresponded to respective sensitivities of 75.00% and 75.00%, and specificities of 87.76% and 91.84%. For tumors of 10–20 mm, the optimal cut-off values were 4.59 m/s and 4.13 m/s for SWV_VTQ and SWV_VTIQ, respectively; corresponding to sensitivities of 92.31% and 84.62%, and specificities of 92.59% and 85.19%. Finally, the cut-off values for SWV_VTQ and SWV_VTIQ in tumors >20 mm were 4.57 m/s and 4.36 m/s, and these represented sensitivities of 91.43% and 94.29%, and specificities of 87.18% and 87.18%.

Optimal cut-off values for SWV_VTQ and SWV_VTIQ were higher for larger tumors, ≥10 mm. In addition, when tumors were over 10 mm, the cut-off values were higher for SWV_VTQ versusSWV_VTIQ.

4 Discussion

The stiffness of a tissue is related to pathological changes and the histological components of any lesions present [20]. Therefore, its measurement allows detection of various diseases that are associated with changes in the mechanical properties of tissue. ARFI is a relatively novel technology fornon-invasive assessment of a tissue’s elastic properties, including stiffness. Its quantitative implementation is called VTQ and this provides an objective numerical value for the shear wave velocity (SWV), which mainly depends on the stiffness of the target tissue [2 , 7]. Another method of shear wave elastography is VTIQ: this was developed from second-generation VTQ technology and provides many advantages, such as a smaller ROI, a wide range, high reliability and betterreproducibility [9].

The mean modulus of elasticity (∼stiffness) is generally much higher in malignant tumors compared with their benign counterparts [10 , 30]; even for 4–5 mm sized nodules [1]. Evans et al. also found that invasive cancers with an ultrasound size of <15 mm had a mean modulus of stiffness of 109 kPa, compared with an average value of 167 kPa for lesions≥15 mm [4]. When using static elasticity imaging, lager breast masses have been found to exhibit higher stiffness scores regardless of whether they were benign or malignant [13]; therefore, in our study we grouped the tumors according to their size, as indicated by B-mode ultrasound imaging.

Our results showed a wide range of SWV_VTQ and SWV_VTIQ values for both benign and malignant tumors so that there is considerable overlap between the benign and malignant values, as is the case with conventional ultrasound. The mean SWV_VTQ and SWV_VTIQ were significantly higher for malignant tumors than for benign tumors in all three size ranges, which is what we expected. The main reason for this difference is the changes to the elastic modulus that occur in pathological tissues. Krouskop et al. used elastography to investigate the mechanical behavior of breast tissue subject to compression loading and found that tissue elastic moduli were ordered as follows: fat <normal glandular tissue <fibrous tissue <non-invasive ductal carcinoma <invasive ductal carcinoma [15]. Benign tumors such as fibroadenoma have loosely arranged tumor cells and more interstitial mucopolysaccharides so that their stiffness values are low. On the other hand, malignant tumors exhibit high stiffness because they contain abundant connective tissue, blood vessels, lymphatic vessels and the tumor cells are surrounded by tightly packed hyperplastic fibrous tissue. In addition, malignant tumors stick to nearby tissue, thereby decreasing their activities. Therefore, we conclude that SWV_VTQ and SWV_VTIQ can serve as good indicators of malignant features in tissue.

Using shear-wave elastography, Ganau et al. found no statistically significant correlations between tissue elasticity parameters and the histological grade or the molecular subtype [8]. In a previous study of ours concerning invasive ductal carcinoma, we found that tumor size was positively associated with SWV, and that invasive size was the strongest pathologic determinant of SWV [28]. For malignant tumors in our current study, SWV measured by either VTQ or VTIQ was significantly higher when they were larger than 10 mm. We suggest that the larger tumors are stiffer because of the increased vascularization they require. The larger the tumor, the greater the invasion into surrounding tissue; leading to increased stability and stiffness. Although the SWVs for very small malignant tumors were relatively low, they were all greater than 4 m/s, which is in line with the values reported by Liu et al. and Ricci et al. [16, 18]. Thus, we strongly recommend that clinicians be more vigilant against tumors that generate SWVs above 4 m/s.

So far, specialists worldwide have not reached an agreement on standard SWV cut-off values for discriminating between malignant and benign tumors. Yao et al. found that the optimal value for VTQ in their study was 3.30 m/s [29]. In our study, we calculated optimal cut-off values for tumors in three different size ranges. Tumors≥10 mm had similar optimal values, and sensitivity and specificity were both at least 80%. Our optimal values for tumors <10 mm (VTQ, 2.94 m/s; VTIQ, 3.78 m/s) were similar to those in some previous studies: 3.09 m/s for VTQ [17] and 3.27 m/s for VTIQ [16], but the sensitivities declined to 75% for both methods. We suggest that the distribution of tumor subtypes in our study is an important influence here and that a large-scale multicenter study could provide more effective cut-off values. Nevertheless, as part of a larger multisource dataset, VTQ and VTIQ results such as ours do provide useful information for identifying malignant breast tissue. At this stage, to reduce missed and erroneous diagnoses, it is best to obtain a plurality of measurement parameters including those from B-mode imaging, Doppler color flow imaging and ARFI-VTQ/VTIQ; especially for very small tumors.

Early breast-cancer studies using VTQ technology indicated that operator dependence can be considered negligible when assessing the stiffness of breast tumors [24]. VTIQ was developed on the basis of VTQ, it uses multi-set push pulse and detection pulse sequences to measure localized SWV over a wide range. VTIQ is not limited to measuring a single point: it can obtain quantitative and qualitative information on the tissue stiffness across multiple locations. Therefore, VTIQ measurements represent the stiffness of the tissue more directly, and theoretically, its diagnostic performance should be superior to VTQ. In our study, we compared the AUCs of the two methods across the three tumor-size ranges and found that both performed very similarly, and at least moderately well (AUC≥0.8), in all groups. This finding is in line with the studies of both Tozaki et al. and Ianculescu et al., which conclude that VTIQ has no significant advantage over VTQ with regard to distinguishing benign and malignant tumors [12, 25]. The AUCs of VTQ and VTIQ in tumors≥10 mm exceeded those in tumors <10 mm. This may relate to the different physical features of small tumors. Thus, very small tumors present an important diagnostic challenge as soft invasive cancers are frequently small (≤10 mm), low grade and screen-detected [27].

VTIQ was not as effective as we expected, but unsuccessful measurements were much more frequent for VTQ, and some malignant tumors displayed X.XX m/s for several measurements. After comparison with the histological results, we found that many of the malignant tumors possessed necrotic and calcified regions. Although we measured each tumor several times and calculated the average SWV, trying to avoid calcifications and cystic regions, the intrinsic flaws of VTQ were difficult to overcome. The reasons may be as follows. First, positioning of the ROI is done blind, so we cannot recognize the necroses and calcifications correctly, particularly in large tumors. Second, VTQ has a narrow range, the upper limit being 8.4 m/s, which is lower than the limit for VTIQ. Third, faint echo produces weak shear wave signals; heterogeneous tissue absorbs a great deal of sound energy so that the echo becomes weak and cannot be detected. Forth, the angle of refraction of the pulse may influence the measurements. Fifth, VTQ is not a static imaging technology. For the operator, it is important to make sure there is no pressure on the target and no shaking. Thus, VTQ cannot consistently provide accurate SWVs for some tissues. By contrast, VTIQ is better in this regard and, as such, is favored by readers and operators.

There were some limitations to our study. The number of samples was relatively small and all cases came from a single hospital. The dimension of the VTQ ROI was fixed, which would limit clinical utility. Almost all the malignant lesions included in our study were invasive ductal carcinomas (76.62%) and other subtypes were rare; this selection bias would affect the results. Finally, the mechanical properties of tissues only conform to the simple models of elastic mechanics in an approximate fashion, limiting the effectiveness of ARFI. In summary, neither VTQ nor VTIQ can take the place of conventional ultrasound and be applied alone for diagnosis of solid breast tumors.

Given the above, VTQ and VTIQ can be considered as valuable complements to conventional ultrasound. Both are feasible and promising methods for discriminating between malignant and benign breast tumors and their clinical diagnostic performances were found to moderate to good. Although the two methods have higher sensitivities in tumors over 10 mm in diameter, their overall diagnostic performances did not change significantly for different sizes of tumor.

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