Comparison of the C-TIRADS, ACR-TIRADS, and ATA guidelines in malignancy risk stratification of thyroid nodules

Introduction

Thyroid nodules are detected in 19–68% of randomly selected individuals, and 7–15% of them are malignant (1). With the rising incidence of thyroid cancer and the development of diagnostic effects, the detection rate of thyroid cancer has risen yearly (2). Many ultrasonic examinations and fine needle aspiration (FNA) have been carried out, which has raised concerns about the overtreatment of thyroid nodules.

Many risk stratification systems have been established to standardize the risk stratification of thyroid lesions and propose corresponding management recommendations, including FNA (1,3-5). Two of them, the Thyroid Imaging Reporting and Data System of the American College of Radiology (ACR-TIRADS) set forth by the American College of Radiology in 2017 and the American Thyroid Association (ATA) guidelines set forth by the ATA in 2015, are widely applied for the diagnosis and treatment of thyroid nodules. Recently, the Superficial Organ and Vascular Ultrasound Group of the Society of Ultrasound in Medicine of the Chinese Medical Association established the 2020 Chinese Thyroid Imaging Reporting and Data System (C-TIRADS) guidelines (6). There are many differences in the analysis of ultrasound (US) images among the three guidelines. The ACR-TIRADS takes advantage of a weighted method to calculate the scores of US signs to predict the malignant risk of thyroid nodules, while the C-TIRADS counts the number of positive and negative signs. The ATA guidelines propose a pattern-based qualitative system defining 5 categories with different risks of malignancy. Additionally, the nodule size thresholds for FNA are different in the three guidelines. These different guidelines for assessing the same thyroid nodule may show different diagnostic performance of malignancy and FNA recommendations. Although some studies (7,8) have been conducted to compare the diagnostic performance of malignancy and FNA recommendations of the three guidelines, further exploration on FNA recommendations has not been undertaken, which prevents us from managing thyroid nodules more effectively. The aim of this study was to compare their diagnostic performance for malignancy and FNA recommendations. We presented this article in accordance with the STARD reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-22-826/rc).

Methods

This is a retrospective study. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the ethics board of the Shantou Central Hospital [ID (2021) scientific research 057], and individual consent for this retrospective analysis was waived. The diagnostic performance of the guidelines is affected by many factors, including the experience of the radiologist and the included sample. In previous studies, the areas under the curve (AUCs) of diagnostic performance in malignant thyroid nodules according to the C-TIRADS, the ACR-TIRADS and the ATA guidelines varied from 0.8 to 0.95, in which the highest remained controversial (9-11). Therefore, we estimated that the AUCs of the guidelines were 0.8 and calculated the sample size that could predict malignancy risk in thyroid nodules. We used PASS v11.0 (NCSS LLC., Kaysville, USA) to estimate the minimal sample size. We chose “Tests for One ROC Curve” in the category, and the analysis was performed with α=0.05 and β=0.1. We set the sample allocation ratio, AUC0 and AUC1 at 1.0, 0.5 and 0.8, respectively. We set the lower false-positive rate and the upper false-positive rate at 0 and 1, respectively. The data were discrete, and the B value was set at 1. A two-sided Z test was adopted. The minimal sample size was 34 and included 17 malignant thyroid nodules.

Patients

We performed a retrospective review on the database in Shantou Central Hospital for patients with thyroid nodules from January 2021 to December 2021. We collected the data in 2022. The participants formed a consecutive series. Patients with the following criteria were included: (I) underwent surgery; (II) definitive histopathological results of target nodules; and (III) an US examination of the thyroid within 3 months before surgery. The exclusion criteria were as follows: (I) the histopathological results of the target nodules were unclear; (II) the target nodules could not be clearly identified on US examination; (III) the patients had undergone radiotherapy or chemotherapy; (IV) the medical records were incomplete; and (V) the patients had insufficient mental development or gravidas. If the patient had more than one thyroid nodule, the one nodule that met the above criteria and had the most high-risk US features in each thyroid lobe or isthmus was included. We chose the histopathological result as a reference standard to make it more convincing. A total of 1,143 patients with 1,376 thyroid nodules underwent an US examination in the last year, while 139 patients with 148 thyroid nodules were excluded due to the lack of histopathological results. A flowchart of the participants is shown in Figure 1.

Figure 1 Flow of the participants.

Analysis of US images

The ultrasonography examinations of the thyroid gland and cervical region were performed with General Electric Voluson E8 (General Electric, Schenectady, USA) and Philips Iu22 (Philips, Amsterdam, Netherlands) equipped with 5–12-MHz linear array transducers. The US images of 1,004 patients with 1,228 nodules who met the above criteria were independently analyzed by two experienced radiologists (L Lu and R Ma) who had engaged in thyroid US diagnosis for more than 10 years. The radiologists were blinded to the histopathologic results of the thyroid nodules. All thyroid nodules were evaluated and categorized according to the 2020 C-TIRADS, the 2017 ACR-TIRADS and the 2015 ATA guidelines. The 2020 C-TIRADS was calculated by adding the number of malignant US features, including vertical orientation, solid composition, hypoechogenicity, microcalcifications and ill-defined/irregular margins or extrathyroidal extension, and subtracting 1 if a negative feature of the comet-tail artifacts was present (6). Based on the 2020 C-TIRADS, the thyroid nodules were classified as C-TIRADS 2 (−1 point), C-TIRADS 3 (0 point), C-TIRADS 4A (1 point), C-TIRADS 4B (2 points), C-TIRADS 4C (3 points) and C-TIRADS 5 (4 points or more). In the 2017 ACR-TIRADS, mixed cystic and solid composition, solid or almost completely solid composition, hyperechoic or isoechoic, hypoechoic, very hypoechoic, vertical orientation, lobulated or irregular margin, extrathyroidal extension, macrocalcifications, peripheral calcifications and microcalcifications were assigned 1, 2, 1, 2, 3, 3, 2, 3, 1, 2 and 3 points, respectively, and the other US features were assigned 0 points. The score of the ACR-TIRADS was calculated by summing the points of the malignant US features that the thyroid nodule contained (5). Similarly, based on the 2017 ACR-TIRADS, the thyroid nodules were classified as ACR-TIRADS 2 (2 points), ACR-TIRADS 3 (3 points), ACR-TIRADS 4A (4 points), ACR-TIRADS 4B (5 points), ACR-TIRADS 4C (6 points) and ACR-TIRADS 5 (7 points or more). In the 2015 ATA guidelines, thyroid nodules with a high suspicion pattern, intermediate suspicion pattern, low suspicion pattern, very low suspicion pattern and benign pattern were assigned 5, 4, 3, 2 and 1 point, respectively. The “not special” pattern of the ATA guidelines was considered a subtype of the indeterminate-suspicion pattern as Yoon et al. had claimed (12) and was assigned 4 points. Diagnostic FNA in the ATA guidelines is recommended for (I) high or intermediate suspicion sonographic pattern: nodules ≥1 cm; (II) low suspicion sonographic pattern: nodules ≥1.5 cm; and (III) very low suspicion sonographic pattern: nodules ≥2 cm. Diagnostic FNA in the ACR-TIRADS is recommended for (I) ACR-TIRADS 5: nodules ≥1 cm; (II) ACR-TIRADS 4A, 4B or 4C: nodules ≥1.5 cm; and (III) ACR-TIRADS 3: nodules ≥2.5 cm. Diagnostic FNA in C-TIRADS is recommended for (I) C-TIRADS 4A: (i) nodules >15 mm; (ii) if nodules are multiple or immediately adjacent to the trachea or recurrent laryngeal nerve, FNA can be considered if the nodule is >10 mm. (II) C-TIRADS 4B: (i) nodules >10 mm; (ii) if nodules are multiple or immediately adjacent to the capsule, trachea, or recurrent laryngeal nerve, FNA can be considered if the nodule is >5 mm. (III) The recommended management of C-TIRADS 4C and C-TIRADS 5 nodules is similar to that of category 4B nodules. However, if there are typical cervical metastatic lymph nodes, then the most suspicious nodules of any size in the ipsilateral thyroid require FNA. Disagreements in the analysis of the US images between the two radiologists were resolved by consensus. The pathologists did not know the scores of the thyroid nodules.

Statistical analysis

Statistical analysis was performed at both the patient level and the nodule level. Data were extracted by two groups of reviewers (Z Xiao and Y Huang, N Lin and L Chen) independently and included the sex of the patients, the age of the patients and the histopathological results of the nodules. Adenomas, nodular goiters, thyroiditis and parathyroid diseases were considered benign, while papillary thyroid carcinomas, follicular thyroid carcinomas, medullary thyroid carcinoma and other carcinomas were considered malignant. There were no missing data on the index test or reference standard result in our study. Extracted data were entered into IBM SPSS v12.0 (IBM Corp., Armonk, USA) and STATA v13.0 (Stata Corp., College Station, USA). Continuous variables with a normal distribution are expressed as the mean ± standard deviation (SD), and those with an abnormal distribution are expressed as the median (interquartile range). The nominal and ordinal variables were expressed as frequencies and proportions. Independent two-sample t-tests and rank-sum tests were used to compare the results in normal distributions and in abnormal distributions, respectively. The areas under the receiver operating characteristic (AUROC) curves were compared by the Z test. The statistical significance was set at P<0.05. The P value was a two-sided test.

The diagnostic performance of the three guidelines was assessed by ROC curve analysis based on the established cutoff values. The sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), accuracy and AUROC were calculated. The number of thyroid nodules recommended for FNA, the malignant detection rate of the FNA recommendations and the unnecessary FNA rates were also calculated. The unnecessary FNA rates and the malignant detection rates of FNA recommendations were calculated using the following equations: unnecessary FNA rate = the number of benign nodules among the recommended FNA nodules/the number of recommended FNA nodules; malignant detection rates of FNA recommendations = the number of malignant nodules among the recommended FNA nodules/the number of recommended FNA nodules. To compare the unnecessary FNA rates of the three guidelines in thyroid nodules of different sizes, subgroups were established according to whether the thyroid nodules were larger than 20 mm. The sensitivity, specificity, PPV, NPV and accuracy of FNA recommendations were calculated based on the three guidelines.

Results

A total of 1,004 patients with 1,228 thyroid nodules were included in the study. The nodules of 724 patients were all benign, and 280 patients had one or more malignant nodules at least. There were 828 females and 176 males, and the median age was 48.00 (38.00, 57.00) years. There were no significant differences in sex or age between the patients with malignant nodules and the patients with benign nodules. A total of 936 nodules were benign, including 304 adenomas, 576 nodular goiters, 50 thyroiditis and 6 parathyroid diseases, and 292 nodules were malignant, including 280 papillary thyroid carcinomas, 11 follicular thyroid carcinomas and 1 medullary thyroid carcinoma. The median size of the included nodules was 25.00 (13.00, 35.00) mm, and the sizes of the benign nodules were significantly larger than the sizes of the malignant nodules [28.50 (18.25, 37.00) vs. 12.00 (8.00, 18.00) mm, P<0.001].

There were many differences in the US features between the malignant nodules and benign nodules. More malignant nodules were solid or purely solid [277 (94.86%) vs. 420 (44.87%), P<0.001], very hypoechoic [63 (21.58%) vs. 19 (2.03%), P<0.001] or hypoechoic [213 (72.95%) vs. 539 (57.59%), P<0.001], immediately adjacent to the capsule, trachea or the recurrent laryngeal nerve [212 (72.60%) vs. 480 (51.28%), P<0.001], with a taller-than-wider shape [92 (31.51%) vs. 25 (2.67%), P<0.001, 103 (35.27%) vs. 29 (3.10%), P<0.001], extrathyroidal extension [28 (9.59%) vs. 6 (0.64%), P<0.001], irregular or lobulated margin [198 (67.81%) vs. 44 (4.70%), P<0.001], microcalcification [166 (56.85%) vs. 45 (4.81%), P<0.001], and typical cervical metastatic lymph nodes (9 (3.08%) vs. 0 (0.00%), P<0.001]. More benign nodules were mixed [495 (52.88%) vs. 15 (5.14%), P<0.001], cystic, purely cystic or spongiform [21 (2.25%) vs. 0 (0.00%), P=0.007], hyperechoic or isoechoic [358 (38.25%) vs. 16 (5.48%), P<0.001], and anechoic [20 (2.13%) vs. 0 (0.00%), P=0.007], had a wider-than-taller shape [911 (97.33%) vs. 200 (68.49%), P<0.001; 907 (96.90%) vs. 189 (64.73%), P<0.001], a smooth or ill-defined margin [886 (94.66%) vs. 66 (22.60%), P<0.001], and no echogenic foci or only large comet-tail artifacts [801 (85.58%) vs. 93 (31.85%), P<0.001]. The basic characteristics of the patients and the US features of the thyroid nodules are shown in Table 1.

Comparison of diagnostic performance of the three guidelines

All thyroid nodules were classified following the three guidelines. The ROC curve shows the diagnostic performance of the three guidelines in Figure 2. As the ROC curve suggested, the C-TIRADS, ACR-TIRADS and ATA guidelines could distinguish malignant nodules from benign nodules with cutoff values of 1.5, 5.5 and 4.5 points, respectively. According to the cutoff value, thyroid nodules were considered malignant nodules if they were classified as 4B, 4C and 5 in the C-TIRADS, 4C and 5 in the ACR-TIRADS and highly suspicious in the ATA guidelines. When the thyroid nodules were classified as 4A or below in the C-TIRADS, 4B or below in the ACR-TIRADS and intermediate suspicion or below in the ATA guidelines, the nodules were regarded as benign. Based on the criteria, the AUROC of the ACR-TIRADS was significantly larger than that of the ATA guidelines (0.938 vs. 0.928, P=0.02). However, the C-TIRADS had no significant difference in the AUROC with the ACR-TIRADS and the ATA guidelines (0.933 vs. 0.938, P=0.24; 0.933 vs. 0.928, P=0.32). The comparison of the diagnostic performance of the three guidelines is shown in Table 2. The ATA guidelines had a higher specificity (93.38% vs. 89.42%, P=0.002; 93.38% vs. 88.68%, P<0.001), accuracy (92.10% vs. 89.41%, P=0.02; 92.10% vs. 89.25%, P=0.02) and PPV (80.56% vs. 72.50%, P=0.01; 80.56% vs. 71.51%, P=0.006) than the C-TIRADS and the ACR-TIRADS. There were no significant differences in the sensitivity (89.38% vs. 91.10%, P=0.49; 91.10% vs. 88.01%, P=0.22; 89.38% vs. 88.01%, P=0.60) and NPV (96.43% vs. 96.96%, P=0.54; 96.96% vs. 96.15%, P=0.35; 96.43% vs. 96.15%, P=0.76) among the three guidelines.

Figure 2 ROC curve of the 2020 C-TIRADS, the 2017 ACR-TIRADS and the 2015 ATA guidelines. The area under ROC: χ²=6.02, P value =0.05; the cutoff value of C-TIRADS =1.5 points; the cutoff value of ACR-TIRADS =5.5 points; the cutoff value of ATA =4.5 points; C-TIRADS, Chinese Thyroid Imaging Reporting and Data System; ACR-TIRADS, Thyroid Imaging Reporting and Data System of the American College of Radiology; ATA, American Thyroid Association guidelines; ROC, receiver operating characteristic.

Comparison of FNA recommendations

According to the C-TIRADS, the number of FNA recommendations was 632, which was significantly less than those based on the ACR-TIRADS (51.47% vs. 57.17%, P<0.001) and the ATA guidelines (51.47% vs. 81.03%, P<0.001). The malignant detection rates (PPVs) of the FNA recommendations of the three guidelines are shown in Table 3. The sensitivity of the FNA recommendations of the C-TIRADS was significantly higher than that of the ACR-TIRADS (84.25% vs. 57.53%, P<0.001) and the ATA guidelines (84.25% vs. 62.67%, P<0.001), while there was no significant difference in the sensitivity of FNA recommendations between the ACR-TIRADS and the ATA guidelines (57.53% vs. 62.67%, P=0.21). The specificity, PPV, NPV and accuracy of FNA recommendations of the C-TIRADS were highest among the three guidelines (58.76%, 38.92%, 92.28% and 64.82%, respectively), followed by the ACR-TIRADS (42.94%, 23.93%, 76.43% and 46.42%, respectively) and the ATA guidelines (13.25%, 18.39%, 53.22% and 25.00%, respectively). The comparison of FNA recommendations of the three guidelines is shown in Table 4. The unnecessary FNA rate based on the C-TIRADS was significantly lower than those based on the ACR-TIRADS and the ATA guidelines (61.08% vs. 76.07%, P<0.001; 61.08% vs. 81.61%, P<0.001). The unnecessary FNA rate of the ACR-TIRADS was significantly lower than that of the ATA guidelines (76.07% vs. 81.61%, P=0.006). In the subgroup (<20 mm), the unnecessary FNA rates of the C-TIRADS and ACR-TIRADS were lower than those of the ATA guidelines (39.16% vs. 54.23%, P<0.001; 32.28% vs. 54.23%, P<0.001), but there was no significant difference in the unnecessary FNA rates between the C-TIRADS and ACR-TIRADS (39.16% vs. 32.28%, P=0.15). In the subgroup (≥20 mm), the unnecessary FNA rate of the C-TIRADS was significantly lower than those of the ACR-TIRADS (82.04% vs. 88.79%, P=0.005) and the ATA guidelines (82.04% vs. 91.29%, P<0.001), but there was no significant difference in the unnecessary FNA rates between the ACR-TIRADS and the ATA guidelines (88.79% vs. 91.29%, P=0.14). The comparison of the unnecessary FNA rates of the three guidelines is shown in Table 5.

Discussion

In our study, we found some low-risk and high-risk features, as previous studies reported. The ratio of malignant thyroid nodules with mixed composition was below that of benign thyroid nodules with mixed composition (5.14% vs. 52.88%, P<0.001), which was concurrent with previous studies (8,13). The mixed composition in the US signs of thyroid nodules was considered to be at risk and assigned 1 point according to the ACR-TIRADS. The results of our study showed that the mixed composition in the US sign of thyroid nodules might have no strong association with malignancy, and its significance in the risk stratification system should be reassessed. In addition, we found no significant difference in the malignant rate between thyroid nodules with a taller-than-wider shape on transverse or longitudinal sections and those with a taller-than-wider shape only on transverse sections (35.27% vs. 31.51%, P=0.91), which contradicts the results of Moon et al. (14). It was necessary to reevaluate whether to assess the vertical orientation of thyroid nodules on both transverse and longitudinal sections. Therefore, future risk stratification systems may need to reassess the significance of these features in distinguishing malignant nodules from benign nodules.

Our study showed that the diagnostic performance of the C-TIRADS was closely comparable to that of the other two guidelines, and the best cutoff value of the C-TIRADS was 1.5 points, which is still controversial. A recent study with a small sample size conducted by Dong et al. (9) demonstrated that the ACR-TIRADS had slightly better diagnostic performance than the C-TIRADS for thyroid nodules. In their study, the cutoff value of the C-TIRADS was 2.5 points, and that of the ACR-TIRADS was 6.5 points, which were different from ours. In their study, the AUROCs of the C-TIRADS and the ACR-TIRADS were 0.806 and 0.843, respectively, which were much lower than those of our study. Some previous studies claimed that the AUROC of the C-TIRADS was significantly higher than those of the ACR-TIRADS and the ATA guidelines (8,15). They set the cutoff value of the C-TIRADS, the ACR-TIRADS and the ATA guidelines at 2.5, 6.5 and 4.5 points, while we set the cutoff value at 1.5, 5.5 and 4.5 points, respectively. All the AUROCs of the three guidelines in their studies were lower than those of our study. We thought the differences in the diagnostic performance between their studies and our study might be associated with the population group being examined, the different cutoff values and the experience of the radiologists. We thought 1.5 points might be a better cutoff value for the C-TIRADS according to our results, which was consistent with the conclusion drawn by Hu et al. (10). In addition, some researchers have recently taken advantage of computer-aided diagnosis technology, which has no operator-dependent inference, to distinguish malignant thyroid nodules from benign thyroid nodules (16-18). The paper published by Bian et al. (16) showed that there was no significant difference in the AUROC between the TIRADS and the ultrasonic S-Detect model (0.94 vs. 0.91, P=0.19), and the ultrasonic S-Detect model performed well in malignancy risk stratification of thyroid nodules. The application of computer-aided diagnosis technology may eliminate subjective factors and help young radiologists predict malignancy risk accurately. All the studies showed that the AUROCs of the C-TIRADS, ACR-TIRADS and ATA guidelines were high, and we could draw a conclusion that the three guidelines could effectively predict the malignancy risk of thyroid nodules.

Thyroid nodules are very common. However, the malignant rate of thyroid nodules is so low that unnecessary FNA should be avoided if possible. Some previous studies claimed that the ACR-TIRADS reduced unnecessary FNA with a higher malignancy detection rate compared with the ATA guidelines, which was consistent with our results (11,19). However, the paper published by Zhu et al. claimed that the fewest thyroid nodules were recommended for FNA according to the ACR-TIRADS, followed by those according to the ATA guidelines and the C-TIRADS (8). In their study, the unnecessary FNA rates of the C-TIRADS were lower than those of the ACR-TIRADS and the ATA guidelines. Our study found that the sensitivity, specificity, PPV, NPV and accuracy of FNA recommendations according to the C-TIRADS were higher than those according to the other two guidelines. The NPV of FNA recommendations according to the C-TIRADS was 92.28%, which was much higher than those according to the other two guidelines. Our results implied that the FNA recommendations of the C-TIRADS could be used to exclude malignancy effectively. On the other hand, lesions that were not recommended for FNA according to the C-TIRADS might be only followed up without biopsy. In our study, the unnecessary FNA rate of the C-TIRADS was even lower than that of the ACR-TIRADS in all nodules and one of the subgroups (≥20 mm), and we found that the unnecessary FNA rates of the three guidelines increased as the thyroid nodules became larger. We concluded that FNA recommendations according to the C-TIRADS might be more efficient than those according to the ACR-TIRADS and the ATA guidelines, especially among larger thyroid nodules. More unnecessary FNA could be avoided based on the FNA recommendations of the C-TIRADS. We thought the efficient FNA recommendations of C-TIRADS were associated with attention to high-suspicion nodules. In our study, the malignant nodules were significantly smaller than the benign nodules. The C-TIRADS pays more attention to high-suspicion nodules that are relatively small and pays less attention to low-suspicion nodules, even though more efficient FNAs can be achieved with them because they are large, especially nodules classified as 4B, 4C or 5, which are recommended for FNA even if they are larger than 5 mm under certain conditions. The paper published by Lin et al. also indicated that the C-TIRADS showed an advantage in reducing unnecessary FNA among patients with follicular neoplasms compared with the ACR-TIRADS and the ATA guidelines (20). However, more randomized controlled trials are needed to confirm our conclusion.

Our study had several limitations. First, all the included nodules were from patients in our hospital who were admitted to surgery, which could not perfectly represent the thyroid nodules in the social population. Second, we chose histopathological results as the diagnostic criteria to improve diagnostic accuracy and excluded nodules that only had cytopathological results, which may lead to selection bias. Third, this study is a retrospective study rather than a randomized trial, which may lead to selection bias. Finally, the FNA results are influenced by many factors, such as nodule size and FNA skill. All the results of the FNAs in our paper were only calculated in theory.

Conclusions

In conclusion, the 2020 C-TIRADS, the 2017 ACR-TIRADS and the 2015 ATA guidelines can efficiently predict malignancy risk in thyroid nodules. Specifically, the C-TIRADS shows the highest sensitivity, specificity, PPV, NPV and accuracy in its FNA recommendations among the three guidelines and offers a reduction in unnecessary FNA and the highest efficacy in distinguishing thyroid carcinoma theoretically. However, the limitations of this study prevent us from reaching a confirmed and general conclusion. More multicenter RCTs with larger sample sizes, long-term follow-up and higher quality are needed to confirm and update the findings of our study.

Acknowledgments

Funding: This work was supported by the Science and Technology Planning Project of Shantou (No. 211114116491861).

Footnote

Reporting Checklist: The authors have completed the STARD reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-22-826/rc).

Conflicts of Interest: All the authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-22-826/coif). All authors report that this study was supported by the Science and Technology Planning Project of Shantou (No. 211114116491861). The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the ethics board of the Shantou Central Hospital [ID (2021) scientific research 057], and individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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