Diagnostic value of ultrasound elastography and conventional ultrasound for thyroid nodules: a meta-analysis
Thyroid nodules are a common clinical problem. According to epidemiological data, 4–7% of the population have accessible thyroid nodules, and 8–16% of thyroid nodules are suspected to be thyroid cancer (1). Penetration is a common examination technique, but this method is subjective and depends mainly on the experience of clinicians. Furthermore, small and deep thyroid nodules are often inaccessible. Compared with palpation, ultrasonography is more sensitive and has high value in the detection and diagnosis of thyroid nodules. Studies have shown that the detection rate of thyroid nodules by ultrasonography in asymptomatic patients was 67% (2). In addition, with the development of high-resolution ultrasound, thyroid nodules of 1.0–2.0 mm can be detected effectively (3).
Ultrasound examination has become the preferred method for the diagnosis of thyroid diseases due to its advantages of simple operation, non-invasiveness, good repeatability and high resolution. In a conventional ultrasound examination, the following features are evaluated for every nodule: echogenicity (hypo- or non-hypoechogenicity with reference to adjacent thyroid parenchyma), echotexture, shape, margin, halo sign, aspect ratio, presence of microcalcifications (hyperechoic spots <2 mm in size, without acoustic shadowing) and nodular vascularisation (4). However, conventional ultrasound examination mainly uses two-dimensional technology, and it has limited value for differentiating between benign and malignant thyroid diseases (5).
In recent years, a range of ultrasound technology has been developed and applied in clinical practice, with good clinical application results. Ultrasonic elastography is a new ultrasonic technology developed in recent years; it was first proposed by Ophir et al. (6) in 1991 and was first applied to thyroid diseases by Lyshchik et al. (7) in 2005. Ultrasound elastography uses the elasticity coefficient of the tumour or other lesion area and the surrounding normal tissue to produce different strain sizes. Colour coding indicates the determined elasticity of the tissue, providing a new direction for the diagnosis of benign and malignant thyroid nodules.
At present, there are many studies on the accuracy of ultrasound elastography for evaluating benign and malignant thyroid nodules, but there is a lack of systematic research. Therefore, this study aimed to systematically evaluate the diagnostic value of conventional ultrasound, ultrasound elastography and conventional ultrasound combined with ultrasound elastography for the differential diagnosis of benign and malignant thyroid micro-nodules to provide objective evidence-based medical evidence on the accuracy of ultrasound elastography for differentiating between benign and malignant thyroid nodules. The following article is presented in accordance with the PRISMA-DTA reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-22-505/rc).
Following the PRISMA guidebook, a systematic literature search of the PubMed, EMBASE, Cochrane Library, Web of Science, CINAHL, China National Knowledge Infrastructure, Wanfang and VIP databases was performed from their date of inception to 30 April 2022. The last time the databases were searched was on 30 May 2022. The search terms included ‘Thyroid nodules’, ‘Ultrasound elastography’ or ‘Elastography’, and ‘Ultrasonography’ or ‘Conventional ultrasonography’. Synonyms of each term were also used.
Inclusion and exclusion criteria
The inclusion criteria were as follows: (I) subjects diagnosed with thyroid nodules, (II) the same group of cases were examined by ultrasound elastography and conventional ultrasound, (III) pathological examination results were used as the gold standard, (IV) four-table information of calculated sensitivity and specificity were obtainable, (V) published in Chinese or English and (VI) a DTA study.
The exclusion criteria were (I) non-population studies, (II) conference articles, case reports, systematic reviews and other research types, (III) insufficient outcome information that could not be analysed, (IV) repeated research reports and (V) the study of complete articles cannot be obtained.
Study selection and data extraction
Two reviewers independently reviewed the abstracts and the full text of each article according to the inclusion and exclusion criteria. In the case of disagreements between the two reviewers, a third reviewer was recruited for discussion until a consensus was reached. After the literature was screened, two reviewers independently and respectively extracted the following information: literature information (year, country, study type), demographic characteristics of the subjects, types of reference standards and diagnostic tools, true positive and false positive diagnosis of thyroid nodules, absolute numbers of true negative and false negative observations, and sensitivity and specificity.
Assessments of quality
The QUADAS-2 scale, developed by Whiting at the University of York, UK, was used to evaluate the quality of the diagnostic tests in a systematic evaluation (8). The scale was used for quality evaluation from four aspects: the selection of research objects, index tests, reference standards, and research process and time. The risks were evaluated according to three risk levels: high risk, low risk and unknown risk.
RevMan 5.3 software was used to evaluate the quality of the diagnostic tests and to plot a bias risk map. Stata 16.0 software was utilised for statistical analysis to calculate the combined sensitivity, specificity; positive likelihood ratio, negative likelihood ratio and their 95% confidence intervals (CI); draw the corresponding summary receiver operating characteristics (SROC) curve and calculate the area under the curve (AUC). A heterogeneity test (I2) was used to determine the size of heterogeneity. If I2<50% or P>0.1, the included literature was considered to be homogeneous. If I2>50% or P≤0.1, the included studies were considered to be heterogeneous. The study type, average age, country, ultrasound elastography criteria and whether conventional ultrasound criteria were clearly pointed out were included in a meta-regression to further explore the factors affecting the sensitivity and specificity of thyroid nodule detection. A value of P<0.05 indicated a statistically significant difference.
After systematic searching and screening, 16 studies (9-24) used pathological examination results as the gold standard to explore the diagnostic value of ultrasound elastography and conventional ultrasound for detecting thyroid nodules. The original research was included in this study. The literature screening process is shown in Figure 1. This study involved 3,280 thyroid nodules, including 999 (30.46%) that were malignant and 2,281 (69.54%) that were benign. Of the 16 studies, 13 were from China (9-20,23) and one each came from Korea (22), Italy (24) and Egypt (21). The average age of the subjects included in the studies ranged from 31.6 to 55.4 years, most of whom were female. In addition, 15 studies (9-18,20-24) reported the absolute number of true positive, false positive, true negative and false negative observations of thyroid nodules detected by conventional ultrasound and ultrasonic elastography, and 9 studies reported the results of thyroid nodule detection by conventional ultrasound combined with ultrasonic elastography. The basic characteristics of the study are detailed in Table 1.
|Study||Country||Study type||Age (years)||Man (%)||Number||The true positive||The false positive||The true negative||The false negative|
|Wu HC, 2010 (9)||China||Retrospective||43.5 [18–81]||45 (18.29)||246||30||34||44||18||14||4||181||185||194||17||13||4|
|Liu L, 2018 (10)||China||Retrospective||43.61±5.18||19 (23.75)||106||17||25||NR||10||2||NR||55||72||NR||24||27||NR|
|Guo MP, 2013 (11)||China||Retrospective||42.3 [19–68]||14 (22.58)||85||19||20||22||4||3||1||44||49||54||18||13||8|
|Jing RF, 2012 (12)||China||Retrospective||49.73±13.37||11 (21.15)||93||23||26||27||6||3||2||54||55||60||10||9||4|
|Li P, 2010 (13)||China||Retrospective||55.4±15.6||9 (21.95)||58||15||17||13||5||6||2||28||28||40||10||7||3|
|Wang W, 2013 (14)||China||Retrospective||31.6 [21–51]||13 (34.21)||49||6||8||NR||2||1||NR||33||38||NR||8||2||NR|
|Han DG, 2011 (15)||China||Retrospective||54 [11–73]||31 (31.63)||129||9||12||NR||12||9||NR||107||99||NR||1||9||NR|
|Liu LL, 2012 (16)||China||Retrospective||18–69||37 (39.78)||126||26||36||40||16||13||7||63||66||71||21||11||8|
|Li HY, 2010 (17)||China||Retrospective||40.76 [23–69]||9 (20.00)||71||17||18||18||4||3||3||47||48||49||3||2||1|
|Sun MY, 2012 (18)||China||Retrospective||48±6||19 (31.15)||84||9||15||NR||8||2||NR||48||59||NR||19||8||NR|
|Shuzhen C, 2012 (19)||China||Retrospective||43.38±0.83||61 (25.00)||291||64||59||NR||2||7||NR||146||191||NR||79||34||NR|
|Yang J, 2017 (20)||China||Retrospective||40 [23–56]||22 (17.89)||150||41||45||NR||9||5||NR||69||86||NR||31||14||NR|
|Shweel M, 2013 (21)||Egypt||Prospective||41±11||12 (25.53)||66||1||12||15||15||4||1||36||42||47||14||8||3|
|Moon HJ, 2012 (22)||Korea||Retrospective||49.7 [18–79]||120 (17.75)||703||199||136||NR||18||81||NR||324||312||NR||162||174||NR|
|Pang T, 2017 (23)||China||Retrospective||44±11||129 (24.57)||525||NR||NR||191||NR||NR||37||NR||NR||266||NR||NR||31|
|Trimboli P, 2012 (24)||Italy||Prospective||53±12.8||138 (31.51)||498||107||102||122||19||24||4||339||231||361||33||41||11|
Con, conventional ultrasound; Ult, ultrasound elastography; Comb, combined diagnosis; NR, not reported.
Literature quality evaluation
The QUADAS-2 quality evaluation results of 16 studies (9-24) are presented in Figures 2,3. The results show that the included studies had a low-risk bias in the selection of subjects and research process and time, and only one study had a high bias in the indicator test. In addition, Figure 2 indicates that the risk bias of the reference standards included some uncertainty.
Sensitivity and specificity
The results of the conventional ultrasound detection of thyroid nodules (Figure 4A) showed a sensitivity of 0.55 (95% CI: 0.45–0.65). The specificity was 0.90 (95% CI: 0.87–0.93), the positive likelihood ratio was 5.8 (95% CI: 3.8–8.9), and the negative likelihood ratio was 0.49 (95% CI: 0.39–0.63). The results of the Q test of sensitivity were P<0.001 and I2=81.88%; the Q test of specificity had values of P<0.001 and I2=79.09%, indicating that there was large heterogeneity between the included studies. The results of the ultrasound elastography detection of thyroid nodules (Figure 4B) showed a sensitivity of 0.67 (95% CI: 0.60–0.73) and a specificity of 0.93 (95% CI: 0.90–0.95). The positive likelihood ratio was 9.1 (95% CI: 6.3–13.3), the negative likelihood ratio was 0.36 (95% CI: 0.29–0.44), the results of the Q test of sensitivity were P<0.001 and I2=86.26%, and those of the Q test of specificity were P<0.001 and I2=87.51%, indicating large heterogeneity in the included studies. The results of the combined detection of thyroid nodules using conventional ultrasound and ultrasound elastography (Figure 4C) revealed a sensitivity of 0.88 (95% CI: 0.84–0.90), a specificity of 0.96 (95% CI: 0.93–0.98), a positive likelihood ratio of 23.3 (95% CI: 12.4–43.6), and a negative likelihood ratio of 0.13 (95% CI: 0.10–0.17). The results of the Q test of sensitivity were P=0.07 and I2=45.26%, and the results of the Q test of specificity were P<0.01 and I2=85.39%, indicating that the included studies had good homogeneity for sensitivity but poor homogeneity for specificity.
The SROC curve
The SROC curve of the conventional ultrasound detection of thyroid nodules (Figure 5A) revealed that the variation in sensitivity was relatively large, and the variation of specificity was relatively stable. The AUC was 0.86 (95% CI: 0.82–0.88). The SROC curve of ultrasonic elastography for detecting thyroid nodules (Figure 5B) showed that the sensitivity had a certain degree of variation, although the variation was significantly less than that of conventional ultrasound. The variation of specificity was stable, and the AUC was 0.89 (95% CI: 0.86–0.91). The SROC curve of conventional ultrasound combined with ultrasound elastography for detecting thyroid nodules (Figure 5C) showed that the sensitivity and specificity of the combined detection method were stable, and the AUC was 0.92 (95% CI: 0.90–0.94), close to the total area of 1.0.
In this study, age, region, type of study, conventional ultrasound criteria and elastography criteria were included in a meta-regression analysis. The results are presented in Table 2.
|Diagnostic methods||Variable||Sensitivity (95% CI)||P||Specificity (95% CI)||P||I2|
|Conventional ultrasound||Age (years)|
|≥50||0.69 (0.54–0.84)||0.06||0.89 (0.83–0.96)||<0.001||64|
|<50||0.50 (0.40–0.60)||0.91 (0.88–0.95)|
|Other||0.45 (0.15–0.76)||0.58||0.87 (0.77–0.97)||0.12||0|
|Asia||0.57 (0.46–0.68)||0.91 (0.88–0.94)|
|Prospective||0.45 (0.15–0.76)||0.58||0.87 (0.77–0.97)||0.12||0|
|Retrospective||0.57 (0.46–0.68)||0.91 (0.88–0.94)|
|Standard for conventional ultrasonic evaluation|
|Not described||0.45 (0.12–0.78)||0.59||0.99 (0.97–1.00)||0.01||83|
|Described||0.56 (0.46–0.66)||0.89 (0.86–0.92)|
|Ultrasound elastography||Age (years)|
|≥50||0.70 (0.61–0.79)||0.01||0.88 (0.82–0.94)||0.01||67|
|<50||0.65 (0.58–0.71)||0.94 (0.92–0.96)|
|Other||0.68 (0.52–0.84)||0.25||0.91 (0.83–0.98)||0.05||0|
|Asia||0.67 (0.60–0.74)||0.93 (0.90–0.96)|
|Prospective||0.68 (0.52–0.84)||0.25||0.91 (0.83–0.98)||0.05||0|
|Retrospective||0.67 (0.60–0.74)||0.93 (0.90–0.96)|
|Evaluation standard of elastic imaging|
|5–point scale||0.71 (0.64–0.79)||<0.001||0.93 (0.90–0.96)||<0.001||32|
|4–point scale||0.61 (0.52–0.70)||0.92 (0.88–0.96)|
|Combined diagnosis||Age (years)|
|≥50||0.88 (0.83–0.93)||<0.001||0.97 (0.93–1.00)||0.07||0|
|<50||0.87 (0.83–0.92)||0.96 (0.93–0.99)|
|Other||0.91 (0.86–0.95)||<0.001||0.99 (0.97–1.00)||<0.001||56|
|Asia||0.86 (0.82–0.90)||0.95 (0.92–0.98)|
|Prospective||0.91 (0.86–0.90)||<0.001||0.99 (0.97–1.00)||<0.001||56|
|Retrospective||0.86 (0.82–0.90)||0.95 (0.92–0.98)|
|Evaluation standard of elastic imaging|
|5–point scale||0.86 (0.82–0.90)||0.01||0.95 (0.93–0.98)||0.34||59|
|4–point scale||0.92 (0.87–0.96)||0.99 (0.97–1.00)|
The results of the conventional ultrasound meta-regression analysis showed that age, region, research type and conventional ultrasound imaging evaluation criteria had no statistically significant effect on the sensitivity of conventional ultrasound in the detection of thyroid nodules. The results of the meta-regression analysis of ultrasonic elastography revealed that age, region, research type and elastography evaluation criteria affected the specificity of ultrasonic elastography, and the influences of region and research type on sensitivity were not statistically significant.
The results of the meta-regression analysis also showed that age, region, research type and elastography criteria affected the sensitivity of the combined diagnosis, and region and research type affected the specificity of the combined diagnosis.
This study systematically evaluated the diagnostic value of conventional ultrasound and ultrasonic elastography in benign and malignant thyroid nodules. The results showed that compared with pathological examination results, conventional ultrasound and ultrasonic elastography provided reasonable and accurate information for the diagnosis of benign and malignant thyroid nodules. The sensitivity of conventional ultrasound was 0.55 (95% CI: 0.45–0.65), the sensitivity of ultrasound elastography was 0.67 (95% CI: 0.60–0.73), and the total sensitivity of the combined diagnosis was 0.88 (95% CI: 0.84–0.90). The AUCs were 0.86, 0.89 and 0.92, respectively. In addition, the results of the meta-regression analysis showed that age, region, research type, conventional ultrasonic evaluation criteria and ultrasonic elastography evaluation criteria had different degrees of influence on sensitivity and specificity.
Conventional ultrasound can diagnose thyroid nodules by comprehensively evaluating the mass’s boundary, morphology, calcification, blood flow and internal echo. However, due to the overlap in the ultrasound imaging of thyroid nodules, the misdiagnosis and missed diagnosis rates may be increased (25). Previous studies have shown that about 30.8% of benign and malignant thyroid nodules had no significant difference in ultrasound images (26).
Ultrasonic elastography provides additional information on tissue hardness compared with conventional ultrasound examination; it can detect deeply located thyroid nodules, compensating for the deficiency of conventional ultrasound examination and improving the objectivity of the diagnosis. There are two main evaluation criteria for ultrasonic elastography. The first is the grade I–IV scoring method, where grades III and above are diagnosed as malignant thyroid nodules (22,24). The second is the 5-point evaluation criteria of Tsukuba University in Japan, in which 4 points and above are the evaluation criteria for malignant thyroid nodules (21,23). The results of the present study suggested that the evaluation criteria affect the sensitivity and specificity of the diagnosis. When using only hyperelastic imaging, the sensitivity and specificity of the 5-point method were higher than those of the 4-point method. In the combined detection method, the sensitivity of the four-point method was higher than the specificity.
The imaging of thyroid nodules is related closely to the pathological characteristics of the nodules. Clinical practice suggests that the ultrasound images of thyroid follicular carcinoma are mostly hypoechoic and parenchymatous masses, which are difficult to identify using routine ultrasound examination. When a nodular goitre is combined with thyroid cancer, ultrasonic elastography might overlap in the detection of tissue hardness (27). Therefore, it is important to use conventional ultrasound combined with ultrasound elastography for the diagnosis of benign and malignant thyroid nodules.
In our study, we showed that the sensitivity and specificity of conventional ultrasound combined with ultrasound elastography for the diagnosis of benign and malignant thyroid nodules were higher than those of a single detection technique, which implies that a combined diagnosis has higher clinical value. As technology improves and society advances, more efficient clinical diagnostic techniques will be developed. For example, the development of an efficient deep convolutional neural network model for the visual localisation and automatic diagnosis of thyroid nodules on ultrasound images has been reported (28).
This study has some limitations. First, due to a lack of sufficient original research, most studies were aimed at the Chinese population and lacked test results from other countries around the world. In terms of literature quality, although the risk of bias in the included studies was low, there was some potential bias in the reference standards. Due to the use of joint diagnostic studies that describe the evaluation criteria of conventional ultrasound, it was not possible to explore the impact of this variable on the results of joint diagnostic tests. Finally, due to the lack of information on the size and location of thyroid nodules, the impact of these variables on diagnostic accuracy could not be explored in depth.
Conventional ultrasound and ultrasound elastography have better sensitivity and specificity for the detection of benign and malignant thyroid nodules. The diagnostic effect of ultrasound elastography is better than that of conventional ultrasound. The diagnostic value of ultrasound elastography combined with conventional ultrasound is higher than that of a single diagnostic method.
We would like to express our gratitude to all those who helped us during the writing of this manuscript. We thank the third-party collaborator for his contribution in reviewing and screening the literature in this study.
Reporting Checklist: The authors have completed the PRISMA-DTA reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-22-505/rc
Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-22-505/coif). The authors have no conflicts of interest to declare.
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