Oncotarget

Meta-Analysis:

Benign and malignant breast lesions identification through the values derived from shear wave elastography: evidence for the meta-analysis

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Oncotarget. 2017; 8:89173-89181. https://doi.org/10.18632/oncotarget.21124

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Yan Xue, Shuxin Yao, Xiaodong Li and Huarong Zhang _

Abstract

Yan Xue1, Shuxin Yao2, Xiaodong Li3 and Huarong Zhang1

1Department of Ultrasonography, Linyi People’s Hospital, Linyi City, Shandong Province 276000, China

2Department of Ultrasonography, Heze Municipal Hospital, Heze City, Shandong Province 274000, China

3Department of Radiology, Linyi People’s Hospital, Linyi City, Shandong Province 276000, China

Correspondence to:

Huarong Zhang, email: nk34odgh@126.com

Keywords: shear wave elastography, diagnose, breast, meta-analysis

Received: April 12, 2017     Accepted: June 30, 2017     Published: September 21, 2017

ABSTRACT

Objective: The analysis was aimed to evaluate the diagnostic accuracy of shear wave elastography (SWE) for malignant breast lesions through a meta-analysis.

Materials and Methods: Related articles were searched in databases of Pubmed, Embase and Cochrane library. Overall sensitivity and specificity were analyzed with DerSimonian and Laird random effects model. Area under curve (AUC) with corresponding 95% confidence interval were also analyzed to evaluate the diagnostic accuracy of SWE. P value < 0.05 predicted the significant heterogeneity between study. Sensitivity and publication bias were assessed as well.

Results: According to the inclusion criteria, 25 articles were selected. In the subgroup analysis, diagnostic sensitivity and specificity of SWE in Asian population were 0.84 (0.79–0.88) and 0.87 (0.84–0.90), respectively, while they were 0.92 (0.86–0.96) and 0.89 (0.84–0.92) in Caucasian population. The diagnostic accuracy of SWE was a little higher for Caucasians than for Asians (0.95 vs. 0.92). The diagnostic sensitivity and specificity of virtual touch tissue quantification (VTTQ) were 0.85 (0.77–0.91) and 0.93 (0.88–0.96), respectively. It showed a little higher value in specificity and summary receiver operating curve (sROC) than that of SWE (0.93 vs. 0.87; 0.95 vs. 0.93). In addition, maximum stiffness exhibited higher detection sensitivity than that of mean stiffness (0.91 vs. 0.85).

Conclusions: SWE serves as an accurate diagnostic technology for discriminating malignant and benign breast lesions.


Benign and malignant breast lesions identification through the values derived from shear wave elastography: evidence for the meta-analysis | Xue | Oncotarget

INTRODUCTION

Breast cancer is one of serious diseases threatening health in women and is also the major cause of death among women [1, 2]. Annually, about 1.38 million new cases and 458, 000 deaths happen worldwide [3]. Moreover, the occurrence rate of this cancer has risen in recent years. Early detection and diagnosis contribute to reducing mortality and improving prognosis. It is urgent to develop efficient detection technology for breast cancer.

Mammographic screening is a valuable tool for early detection of breast cancer [4]. However, the increase in breast tissue density significantly reduces the diagnostic accuracy [5]. Among other imaging methods, gray-scale ultrasonography is a valuable adjunct technique. It shows highly sensitive detection of benign breast lesions from malignant ones [68]. The Breast Imaging Reporting and Data System (BI-RADS) along with ultrasonography contribute to understanding the standardized terminology about ultrasonography features, assessments and recommendations [9, 10]. Nevertheless, this technique is subjective and poorly specific [1012]. Ultrasound elastography emerges as an efficient tool to detect malignant solid lesions through measuring the stiffness. It exhibits 86.5% sensitivity, 89.8% specificity and 88.3% accuracy in discriminating benign and malignant breast lesions [13]. In the ultrasound elastography test, the performance was conducted with freehand compression. The elasticity map largely depends on the the extent of tissue compression and organ’s compressibility limits. Moreover, the differences in skill of the operator may result in distinct results.

Shear wave elastography (SWE), a newly developed technology, could overcome these above mentioned problems. It is performed by remotely inducing mechanical vibrations via acoustic radiation force produced by a focused ultrasound beam. The displacement induced at the focus produces shear wave which delivers information about viscoelastic properties of the tissue, thus generates the quantitative assessment to elasticity values. Until now, there has been many studies investigating the diagnostic role of SWE in discriminating benign and malignant breast lesions, however, no consistent results were obtained.

The meta-analysis was initiated to get more accurate results, which contributes to the early diagnosis of breast cancer and improvement on the treatments.

MATERIALS AND METHODS

Article retrieval

The articles were retrieved in Pubmed, Embase and Cochrane databases. The following search terms were used to retrieve articles: “shear wave elastography”, “SWE”, “acoustic radiation force impulse”, “ARFI”, “virtual touch tissue quantification (VTTQ)”, “VTTQ” and “breast”. The references of retrieved articles were carefully checked for potential ones. Only the articles in English were considered.

Inclusion criteria

The studies were included if they met the following criteria: (1) The study investigated the role of SWE in the diagnosis of malignant and benign breast lesions. (2) Pathological biopsy or cytological (fine-needle aspiration) test was adopted as gold standard. (3) The data of true-positive (TP), false-positive (FP), false-negative (FP) and true-negative (TN) were provided. The study with larger sample size was included for the studies with overlapping data.

Information extraction

The following information was extracted by two independent authors: name of first author, sample size, number of breast lesions, number of malignant and benign breast lesions, gold standard, SWE parameters, TP, FP, FN and TN. The ambiguity was solved with discussion.

Statistics

All the analysis was completed in Stata 12.0 (StataCorp LP, College Station, TX, USA) software. Summary sensitivity and specificity were estimated with DerSimonian and Laird random effects model. Besides, summary receiver operating characteristic (sROC) curve was created according to the odds ratios (ORs) weight of sensitivity and specificity. Meanwhile, area under curve (AUC) with corresponding 95% confidence interval (CI) was analyzed to evaluate the diagnostic accuracy of SWE. P value was adopted to evaluate the heterogeneity between studies. P < 0.05 indicated significant heterogeneity. Deek’s funnel plot was used to assess the publication bias. Subgroup analysis based on ethnicity, technology and SWE parameters (maximum stiffness, mean stiffness and stiffness ratio) were also conducted.

RESULTS

Studies selection and characteristics of included studies

The retrieved studies were selected according to inclusion criteria. The selection process was showed in Figure 1. Total of 188 studies were retrieved from databases. Then, 124 studies were excluded for combination of SWE and other technology, review studies, not SWE analysis and comparison with SWE and other technology. Finally, 25 studies [1438] were included after exclusion of studies for without available data and virtual touch tissue imaging (VTTI) analysis (Table 1). The meta-analysis included 4128 patients and 4546 breast lesions. In the present meta-analysis, 18 articles were for Asian population, while 7 for Caucasian population. 6 articles were based on virtual touch tissue quantification (VTTQ) technology and 19 based on SWE. In the articles of SWE, 13 articles adopted maximum stiffness and 10 adopted mean stiffness.

Flow chart of articles selection.

Figure 1: Flow chart of articles selection.

Table 1: Basic characteristics of included studies

Author

Year

Country

Patients, n

Lesion,n

Benign, n

Malignant,n

Gold standard

Technology

Parameters

Lo

2015

China

81

88

57

31

Pathology

SWE

-

Xiao

2014

China

93

125

81

44

Pathology

SWE

-

Sobczak

2015

Poland

76

84

43

41

Pathology

SWE

Emean

Zhang

2015

China

125

161

106

55

Pathology

SWE

Emax

Klotz

2014

France

142

167

65

102

Pathology

SWE

Emax, Emean

Au

2014

Canada

112

123

79

44

Pathology

SWE

Emax, Emean, Eratio

Yao

2014

China

146

206

163

43

Pathology

VTTQ

SWV

Olgun

2014

Turkey

109

115

83

32

Pathology

SWE

Emax, Emean, Emin, Eratio

Zhou

2014

China

193

193

137

56

Pathology

SWE

Emax, Emean, Emin

Bai

2012

China

108

143

102

41

Pathology

VTTQ

SWV

Jin

2012

China

95

122

66

56

Pathology

VTTQ

SWV

Meng

2011

China

86

92

65

27

Pathology

VTTQ

-

Tamaki

2013

Japan

180

182

26

156

Pathology

VTTQ

-

Tozaki

2012

Japan

158

161

70

91

Pathology

VTTQ

SWV

Evans

2010

UK

52

53

23

30

Pathology

SWE

Emax, Emean, SD

Chang

2011

Korea

158

182

93

89

Pathology

SWE

Emean

Berg

2012

England

939

939

650

289

Pathology

SWE

Emax

Chang

2013

Korea

129

150

79

71

Pathology

SWE

-

Gweon

2013

Korea

119

133

97

36

Pathology

SWE

SD

Lee-a

2013

Korea

139

156

120

36

Pathology

SWE

Emax

Lee-b

2013

Korea

134

144

77

67

Pathology

SWE

Emax, Emean, Eratio

Yoon-a

2013

Korea

199

222

175

47

Pathology

SWE

Emax

Yoon-b

2013

Korea

236

267

208

59

Pathology

SWE

Emax, Emean, Eratio

Youk

2013

Korea

146

163

115

48

Pathology

SWE

Emax

Evans

2012

UK

173

175

64

111

Pathology

SWE

Emax, Emean

Note: maximum stiffness, Emax; mean stiffness, Emean; minimum stiffness, Emin; standard deviation, SD; ratio of stiffness of the mass to the background, Eratio; shear wave velocity, SWV; VTTQ, virtual touch tissue quantification; SWE, shear wave elastography.

Summary sensitivity and specificity analysis

The diagnostic sensitivity and specificity of SWE were analyzed, and the results focused on the subgroup analysis based on ethnicity, technology and SWE parameters in Table 2 and Figures 2, 3. In the analysis of ethnicity, the detection sensitivity and specificity of SWE in Asian population were 0.84 (0.79–0.88) and 0.87 (0.84–0.90), the data in Caucasians were 0.92 (0.86–0.96) and 0.89 (0.84–0.92) (Figure 2). So the detection sensitivity and specificity of SWE in Caucasians were higher than that in Asians. According to SROC, AUC was 0.92 (0.90–0.94) in Asians and 0.95 (0.93–0.97) in Caucasians (Figure 4). Therefore, we found that the accuracy rate of diagnosis of SWE in benign and malignant breast lesions identification was also higher in Caucasian than in Asian populations. The subgroup analysis by technology, the results showed the detection sensitivity and specificity of VTTQ were 0.85 (0.77–0.91) and 0.93 (0.88–0.96), meanwhile, the detection sensitivity and specificity of SWE were 0.88 (0.84–0.91) and 0.87 (0.84–0.89) (Figure 3) respectively. We can see the detection sensitivity of SWE was high, but the specificity was low, compared with VTTQ. Based on SROC, AUC of VTTQ was 0.95 (0.93–0.97) and in SWE was 0.93 (0.90–0.95). the accuracy rate of diagnosis of VTTQ was slightly higher than that of SWE, but the difference was not significant. In addition, we investigated the diagnostic role of SWE parameters (maximum stiffness, mean stiffness and stiffness ratio). According to our synthesized data, maximum stiffness exhibited higher detection sensitivity than both stiffness ratio and mean stiffness (0.91 vs. 0.88 vs. 0.85, respectively); while stiffness ratio showed higher specificity than maximum stiffness and mean stiffness (0.88 vs. 0.84 for both comparisons).

Table 2: Subgroup analysis of meta-analysis

Subgroup

Sensitivity (95% CI)

Ph

Specificity (95% CI)

Ph

Ethnicity

Asian

0.84 (0.79–0.88)

0.00

0.87 (0.84–0.90)

0.00

Caucasian

0.92 (0.86–0.96)

0.00

0.89 (0.84–0.92)

0.00

Technology

SWE

0.88 (0.84–0.91)

0.00

0.87 (0.84–0.89)

0.00

VTTQ

0.85 (0.77–0.91)

0.00

0.93 (0.88–0.96)

0.00

SWE Parameters

Emax

0.91 (0.87–0.94)

0.00

0.84 (0.80–0.87)

0.00

Emean

0.85 (0.71–0.93)

0.00

0.84 (0.79–0.88)

0.01

Eratio

0.88 (0.80–0.93)

0.02

0.88 (0.77–0.94)

0.00

Notes: Ph, P value for heterogeneity.

Analysis of the capability for SWE in discriminating breast malignant lesions from benign lesions in subgroup analysis by ethnicity.

Figure 2: Analysis of the capability for SWE in discriminating breast malignant lesions from benign lesions in subgroup analysis by ethnicity. (A) Sensitivity [0.84 (0.79–0.88)] and specificity [0.87 (0.84–0.90)] in Asian population. (B) Sensitivity [0.92 (0.86–0.96)] and specificity [0.89 (0.84–0.92)] in Caucasian population. SWE shows higher sensitivity and specificity in Caucasians than in Asians.

Analysis of the capability for SWE in discriminating breast malignant lesions from benign lesions in subgroup analysis by technology.

Figure 3: Analysis of the capability for SWE in discriminating breast malignant lesions from benign lesions in subgroup analysis by technology. (A) Sensitivity [0.85 (0.77–0.91)] and specificity [0.93 (0.88–0.96)] for VTTQ. (B) Sensitivity [0.88 (0.84–0.91)] and specificity [0.87 (0.84–0.89)] for SWE. VTTQ shows lower diagnostic sensitivity than SWE, but demonstrates higher specificity than SWE.

SROC analysis in subgroup analysis by technology.

Figure 4: SROC analysis in subgroup analysis by technology. (A) SROC results for VTTQ. (B) SROC results for SWE. The value of AUC is higher for VTTQ [0.95 (0.93–0.97)] than for SWE [0.93 (0.90–0.95)].

Sensitivity and publication bias analysis

Sensitivity analysis was performed by deleting one study each time to observe the changes of results. The analysis indicated that the results were stable. Moreover, no publication bias was found in the meta-analysis (VTTQ: P = 0.216; SWE: P = 0.08, Figure 5).

Deek&#x2019;s funnel plot in subgroup analysis of technology.

Figure 5: Deek’s funnel plot in subgroup analysis of technology. (A) Funnel plot for VTTQ (P = 0.216). (B) Funnel plot of SWE (P = 0.080).

DISCUSSION

SWE is a highly reproducible technology [39]. It determines the propagation velocity of shear waves within the tissues to quantify the stiffness in kPa or m/s [29, 40]. Many tissue elasticity characters can be determined within the region-of-interest (ROI), including maximum (Emax), mean (Emean) and minimum (Emin) stiffness, standard deviation (SD) and ratio of stiffness of the mass to the background (Eratio). Qualitative SWE pattern classification is also reported to show good diagnostic performances [30, 32]. Emax and Emean refers to the general stiffness of the mass, while Eratio represent the relative stiffness of the mass to the fat tissue, the elasticity value of which is 3 kPa [28]. SD and pattern classification illustrate the internal heterogeneity of the mass [32], as the malignant masses are almost histologically heterogeneous. The quantitative measurements of SWE have been recognized as more objective information about the breast mass [39, 40].

Among the included studies, the evaluation about SWE in discriminating malignant and benign breast lesions was controversial. In the study of Zhou et al. [22], 193 women with 193 breast lesions were included to analyze the diagnostic performance of SWE in discriminating benign and malignant breast lesions, in which Emax, Emean and Emin were adopted to represent tissue stiffness. However, the diagnostic sensitivity (0.52, 0.55 and 0.77) and specificity (0.86, 0.78 and 0.78) of these three parameters were all low compared with other studies. Meanwhile, Youk et al. [37] reported high detection sensitivity (0.92) and specificity (0.92) of SWE, in which Emax represent tissue elasticity. Evans et al. (2012) [38] found that the detection sensitivity of SWE was 0.97 (0.92–0.99), while specificity was only 0.69 (0.56–0.80). On the contrary, Evans et al. (2010) [28] reported 0.53 detection sensitivity and 0.83 detection specificity. The variances in results may lie on the differences in characters of patients, ethnicity or SWE parameters.

Subgroup analysis based on ethnicity, technology and SWE parameters was performed in our analysis. The diagnostic sensitivity, specificity and AUC of SWE in Caucasian population were all higher than in Asian population. As we all know, acoustic radiation force impulse (ARFI) includes VTTI and VTTQ. The result of VTTI is featured by elastographic image, while the result of VTTQ is quantitated by SWV (m/s). Soft tissue shows slow SWV, compared to hard tissue [41]. VTTQ has been used for diagnosis in thyroid, prostate, pancreas, liver and breast [4246]. In our study, subgroup analysis according to technology (VTTQ and SWE) was conducted. VTTQ showed higher detection specificity and accuracy than SWE, but its sensitivity was lower than SWE. So, the result is usually unsatisfactory using single technique for breast lesions identification and combination of SWE and VTTQ may be a good technique. In terms of SWE parameters, Emax showed higher diagnostic sensitivity than Emean and Eratio, and Eratio possessed higher specificity than the other two parameters.

Due to the different study population, sample size, exploration factors or examinee-level errors of measurement, the diagnosis results presented in every eligible study were inconsistent. Thus the meta-analysis was the common method to solve the controversy as much as possible. This meta-analysis was based on 4128 patients and 4546 breast lesions. The results were reliable and stable. However, some defects must be pointed out. The number of articles based on Caucasian population was much less than that of Asian population. The accuracy of results on Caucasian population might be affected. In our analysis, the performance of SWE seemed to be better in Caucasians than in Asians, especially for sensitivity, and this phenomenon need to be explored in future special researches, considering the interested topic and space limitation in the present meta-analysis. In previous study, the diagnosis technique of breast lesions distinguish was also different by ethnicity. The diagnostic accuracy of breast lesions based on ultrasound elastography (UE) was 88.4% in Japanese [47] and the percentage was 80.6% in Chinese. Therefore, the diagnosis accuracy difference of the same technique by different races have to be allowed to exist because of variant genetic background and relative environmental factors. In addition, there existed significant heterogeneity between studies. The heterogeneity might result from multiple internal and external factors, such as different threshold values adopted in individual studies, uneven patients’ number, various basic features of patients and diverse test conditions. However, limited to confined information from our included studies, further subgroup analyses based on age and other potentially relevant factors were not performed, so possible sources for the heterogeneity were not identified in this meta-analysis.

Our meta-analysis demonstrates that SWE is an accurate and reliable diagnostic tool in discriminating malignant and benign breast lesions. The outcome is significant in clinic, which contributes to the early diagnostic of breast cancer.

ACKNOWLEDGMENTS

None.

CONFLICTS OF INTEREST

None.

GRANT SUPPORT

None.

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