- Original Article
- Open Access
An updated systematic review of radiomics in osteosarcoma: utilizing CLAIM to adapt the increasing trend of deep learning application in radiomics
Insights into Imaging volume 13, Article number: 138 (2022)
To update the systematic review of radiomics in osteosarcoma.
PubMed, Embase, Web of Science, China National Knowledge Infrastructure, and Wanfang Data were searched to identify articles on osteosarcoma radiomics until May 15, 2022. The studies were assessed by Radiomics Quality Score (RQS), Transparent Reporting of a multivariable prediction model for Individual Prognosis Or Diagnosis (TRIPOD) statement, Checklist for Artificial Intelligence in Medical Imaging (CLAIM), and modified Quality Assessment of Diagnostic Accuracy Studies (QUADAS-2) tool. The evidence supporting radiomics application for osteosarcoma was rated according to meta-analysis results.
Twenty-nine articles were included. The average of the ideal percentage of RQS, the TRIPOD adherence rate and the CLAIM adherence rate were 29.2%, 59.2%, and 63.7%, respectively. RQS identified a radiomics-specific issue of phantom study. TRIPOD addressed deficiency in blindness of assessment. CLAIM and TRIPOD both pointed out shortness in missing data handling and sample size or power calculation. CLAIM identified extra disadvantages in data de-identification and failure analysis. External validation and open science were emphasized by all the above three tools. The risk of bias and applicability concerns were mainly related to the index test. The meta-analysis of radiomics predicting neoadjuvant chemotherapy response by MRI presented a diagnostic odds ratio (95% confidence interval) of 28.83 (10.27–80.95) on testing datasets and was rated as weak evidence.
The quality of osteosarcoma radiomics studies is insufficient. More investigation is needed before using radiomics to optimize osteosarcoma treatment. CLAIM is recommended to guide the design and reporting of radiomics research.
The MRI-radiomics in predicting neoadjuvant chemotherapy response is supported by weak evidence.
The quality of osteosarcoma radiomics studies has been improved recent two years.
CLAIM can adapt the increasing trend of deep learning application in radiomics.
Osteosarcoma is the most common primary high-grade sarcoma of the skeleton, in which the tumor cells produce neoplastic bone . Imaging is the key examination in the work-up of osteosarcoma management, from diagnosis, staging, treatment evaluation, to follow-up [1,2,3]. The diagnosis of osteosarcoma generally starts with X-ray radiography and is followed by CT for further evaluation. A contrast-enhanced MRI scan is useful in diagnosis completion and soft tissue involvement assessment and is usually the last step before biopsy of local disease. A chest CT scan is substantial for lung metastases detection. For patients with pathologically confirmed osteosarcoma, a whole-body PET examination has been recommended for initial staging rather than a bone scintigraphy nowadays. The treatment evaluation and follow-up imaging commonly include local CT and MRI scans and chest CT scan. In most cases, the current imaging approach with physical, laboratory, and histopathological examinations can guide clinicians to an appropriate curation plan, but there remain difficulties in differential diagnosis of osteosarcoma subtypes, prediction of response to treatment, and prognosis concerns including survival, recurrence, and lung metastasis [2, 3]. Radiomics, utilizing a plethora of strategies for extracting underlying information from medical images, has been used to overcome such challenges [4,5,6,7]. Radiomics models have been deemed as a promising approach for addressing clinical problems related to osteosarcoma patients, especially for predicting their response to neoadjuvant chemotherapy (NAC) .
Our preliminary search suggested that radiomics studies in osteosarcoma patients have doubled since the publication of the previous review , indicating necessity for updates on this rapidly developing field. It is unclear whether the radiomics study quality has improved in recent years. Next, the study quality and risk of bias of radiomics research on osteosarcoma have been only assessed by the Radiomics Quality Score (RQS)  and the modified Quality Assessment of Diagnostic Accuracy Studies (QUADAS-2) tool . An additional evaluation using the Transparent Reporting of a multivariable prediction model for Individual Prognosis Or Diagnosis (TRIPOD) checklist  has been recommended to identify several significant items for reporting transparency of radiomics studies [11,12,13,14]. Further, RQS and TRIPOD may not be totally suitable for current radiomics studies, since recently developed deep radiomics applies convolutional neural networks to analyze these extracted features [15,16,17,18]. The Checklist for Artificial Intelligence in Medical Imaging (CLAIM)  has been demonstrated as a useful tool to improve design and reporting of deep learning research [20, 21]. It is potentially better for the evaluation of current radiomics studies with increasing application of deep learning. Finally, the level of evidence supporting the radiomics application in osteosarcoma has not been evaluated yet . It is of importance to provide an overall evidence strength rating before translating radiomics into clinical practice [23, 24]. Therefore, we hypothesized that the publication of the previous review could improve the radiomics study quality in osteosarcoma, and that CLAIM is a better tool for current radiomics studies.
The aim of the present study is to provide an updated systematic review of radiomics in osteosarcoma with quality assessment and evidence-level rating and find out whether CLAIM can better identify disadvantages in current radiomics studies.
Protocol and registration
The updating of this systematic review was decided according to a three-step decision framework  and was conducted in the style of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement . The review protocol (CRD42020175383) and updating information are present in Additional file 1: Note S1. The PRISMA checklist for current systematic review and meta-analysis is present as Additional file 2.
Literature search and selection
An up-to-date literature search was performed via PubMed, Embase, Web of Science, China National Knowledge Infrastructure, and Wanfang Data until May 15, 2022, by two reviewers each with 4 years’ experience in radiology and radiomics research. Disagreements were solved by a review group consisting of radiologists, orthopedists, and pathologists with different levels of experience. All primary research assessing the role of radiomics in osteosarcoma treatment for diagnostic, prognostic, or predictive purposes was considered eligible for the current review. No publication period restrictions were applied, while only articles in English, Japanese, Chinese, German or French were available. The two reviewers screened the titles and abstracts after the removal of duplications and obtained the full-texts and their supplementary materials. The same reviewers determined their eligibility according to the inclusion and exclusion criteria. Other potentially eligible articles were identified from the reference lists of relevant articles and reviews. For uncertainties, the review group was consulted. The search and selection strategy is shown in Additional file 1: Note S2.
Data extraction and quality assessment
We used a data collection sheet for bibliographical information, study characteristics, radiomics considerations, and model metrics (Additional file 1: Table S1) . The eligible studies employed RQS , TRIPOD , CLAIM , and QUADAS-2 tools  (Additional file 1: Tables S2–S5). The RQS is a consensus list composed of sixteen items for methodological issues specific to radiomics studies and is later summarized to six key domains [12,13,14]. The TRIPOD statement provides a checklist consisting of thirty-seven items in twenty-two criteria aiming to promote transparency of prediction model studies and is recommended for identifying room of improvement in radiomics studies [12,13,14]. The CLAIM includes forty-two items in seven topics that should be viewed as a best practice to guide presentation of AI research . The CLAIM has seldomly been employed for quality assessment of radiomics studies [20, 21]. However, we assumed that CLAIM is suitable for radiomics studies evaluation, as radiomics is a subset of AI application in medical imaging [15,16,17,18]. The QUADAS-2 tool was tailored to our review by modifying the signaling questions . Two reviewers independently extracted the data and evaluated the studies. Disagreements were solved by discussion with the review group. Topics discussed are recorded in Additional file 1: Note S3.
Data synthesis and analysis
The statistical analysis was performed with R language version 4.1.3 within RStudio version 1.4.1106 . The RQS rating, the ideal percentage of RQS, and adherence rates of RQS, TRIPOD and CLIAM were calculated. In case a score of at least one point for each item was obtained without minus points, it was considered to have basic adherence, as those have been reported [12,13,14]. For example, if the item of validation in RQS obtained 2–5 points, it was considered as basic adherent, while it was regarded as without basic adherence when it was rated as -5 points. The QUADAS-2 assessment result was summarized. Pearson correlation test was used for the correlation analysis between the ideal percentage of RQS, the TRIPOD adherence rate and the CLAIM adherence rate. Subgroup analysis was performed to compare the ideal percentage of RQS, the TRIPOD adherence rate and the CLAIM adherence rate by journal type, first authorship, imaging modality, and publication period. A two-tailed p value < 0.05 indicated statistical significance, unless otherwise specified. Post hoc multiple comparisons were adjusted using the Bonferroni method. The detailed data analysis method is described in Additional file 1: Note S4.
The meta-analysis was performed using Stata software version 15.1 . In the current systematic review, the role of MRI-driven radiomics in prediction of osteosarcoma patients’ response to NAC was addressed repeatedly. To present the true performance of the radiomics model, corresponding meta-analysis was conducted based on results of testing datasets. The two-by-two tables were directly extracted from the articles or reconstructed based on available data. The diagnostic odds ratio (DOR) with 95% confidence interval (CI) and corresponding p value were calculated using the random-effect model. Sensitivity, specificity, positive and negative likelihood ratio were estimated. A summary receiver operating characteristic (SROC) curve was drawn. The Cochran’s Q test and the Higgins I2 test were used for heterogeneity assessment. The funnel plot was drawn with Egger’s test and Begg’s test, and the Deeks’ funnel plot was constructed with Deeks’ funnel plot asymmetry test for publication bias. A two-tailed p value > 0.10 indicated a low publication bias. The trim and fill method was employed to estimate the number of missing studies. The level of evidence supporting the clinical application of radiomics in osteosarcoma was rated based on results of meta-analysis (Additional file 1: Table S6) .
The search yielded 251 records in total, in which 142 remained after removing duplicates. After screening the titles and abstracts, full-texts of 47 articles were retrieved and reviewed. Ultimately, 29 articles were included in this systematic review [29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57] (Fig. 1). No additional eligible study was identified through hand search of relevant reviews and reference lists of eligible articles.
Table 1 and Fig. 2 summarized the characteristics of 33 models described in the 29 included studies. The sample size of studies ranged from 17 to 191 patients with a median of 81 patients. More than a half of studies were published on non-imaging journals (55.2%), while the majority of first authorship belonged to radiologists (65.5%). The most utilized imaging modality was MRI (48.3%). Almost half of the models aimed to predict the response to NAC (48.5%), followed by prognostic models for survival (18.2%) and those for recurrence or metastasis (9.1%). Most models were validated within the same data with or without resampling (48.5%), while a limited number of models were externally validated (12.1%). The detailed characteristics of studies are present in Additional file 1: Tables S7–S10.
Figure 3 summarized the results of study quality evaluation. Table 2 showed that the median (range) of RQS for current osteosarcoma radiomics studies was 10 (3–18), with a percentage of the ideal score of 29.2% (305/1044) and the adherence rate of 44.6% (207/464). Tables 3 and 4 presented that the TRIPOD and CLAIM adherence rates were 59.2% (481/812) and 63.7% (961/1508), respectively. The risk of bias and applicability concerns were mainly related to the index test. The individual assessment for each study is present in Additional file 1: Tables S11–S14.
RQS addressed a radiomics-specific issue of phantom study (0.0%) and the deficiency in cut-off analysis (0.0%) and cost-effectiveness analysis (0.0%). TRIPOD emphasized the shortness in reporting title (6.9%), blindness of assessment for outcomes and predictors (10.3%; 13.7%), and stating study objective in introduction (24.1%). Both RQS and CLAIM indicated a low percentage of comparing the model with the benchmark (27.6%; 27.6%), while both TRIPOD and CLAIM pointed out the disadvantages in sample size or power calculation (10.3%; 13.7%), and missing data handling (20.7%; 20.7%). CLAIM identified extra lacking in reporting in data de-identification (10.3%), stating study hypothesis in introduction (13.8%), and failure analysis (17.2%). All the above three tools emphasized the validation (25/145, 17.2%; 32/64, 50.0%; 16/29, 55.2%) and open science or additional information (10/116, 8.6%; 6/58, 10.3%; 6/87, 6.9%). The correlation between RQS and TRIPOD (r = 0.7498, p < 0.001) was moderate, while that between TRIPOD and CLAIM (r = 0.9004, p < 0.001) and that between RQS and CLAIM (r = 0.8158, p < 0.001) were high (Additional file 1: Fig. S1).
Figure 4 presents results of study quality evaluation with impact factor, sample size, and publication year. We compared the quality of studies published before and after the previous review and found that the ideal percentage of RQS (22.7% vs 33.8%, p = 0.020), the TRIPOD adherence rate (53.6% vs 63.4%, p = 0.026), and the CLAIM adherence rate (56.1% vs 69.1%, p = 0.007) have all been improved (Additional file 1: Table S15 and Additional file 1: Fig. S2). Subgroup analysis also found that imaging modalities utilized in studies have influence on TRIPOD and CLAIM adherence rates (p = 0.002, p = 0.004). The journal type and first authorship did not significantly influence study quality (both p > 0.05).
The meta-analysis of radiomics predicting NAC response by MRI presented a DOR of 28.83 (95%CI 10.27–80.95) on testing datasets of 115 osteosarcoma patients in total [35, 39, 55, 57] (Fig. 5). The corresponding metrics indicates a dramatic performance (Additional file 1: Figs. S3–S7). The Cochran’s Q test (Q = 5.18, p = 0.160) and Higgins I-square statistic (I2 = 42.04%) indicated that the heterogeneity was moderate. The funnel plot with Egger’s test (p = 0.035) and Begg’s test (p = 0.089) and the Deeks' funnel plot with Deeks’ asymmetry test (p = 0.069) revealed that the likelihood of publication bias was high (Additional file 1: Figs. S8–S9). The trim and fill analysis estimated that two studies were missing (Additional file 1: Fig. S10). However, the adjusted DOR was 20.53 (95%CI 7.80–54.06; p < 0.001). The level of evidence supporting the application of radiomics in predicting NAC response by MRI is rated as weak (Table 5). All meta-analyzed data are presented in Additional file 1: Table S16.
We provided an updated systematic review on osteosarcoma radiomics. Although the overall methodological and reporting quality of included studies was still suboptimal, it has improved after the publication of the previous review. The evidence supporting MRI-driven radiomics to predict NAC response in osteosarcoma has been rated as weak based on meta-analysis of testing data. CLAIM has shown unique ability in capturing deficiency in radiomics studies with deep learning.
In the previous review, the most frequently investigated question was whether radiomics could predict the NAC response , and it is still the most attractive topic nowadays in osteosarcoma radiomics [29,30,31,32, 35, 38,39,40,41,42,43,44, 49, 53, 55, 57]. The current review identified two studies each for differential diagnosis [37, 54], for metastasis at diagnosis [46, 47], and for early recurrence [33, 34] of osteosarcoma, while none of the previous twelve studies touched upon these topics. These achievements cover the routine for osteosarcoma and have potential in aiding clinicians to improve their treatment decision. MRI is currently the most frequently utilized imaging modality, and CT has exceeded PET to become the second. In terms of MRI techniques, T1 mapping and dynamic contrast-enhanced MRI have been introduced into osteosarcoma radiomics studies [31, 55]. However, whether these advanced techniques allow radiomics to better answer the clinical questions has not been fully investigated. Although most of studies segmented ROIs manually, two studies and one study, respectively, employed the region growing method based on the threshold of SUV [40, 42] and a deep learning nnU-Net  for automatic segmentation. These approaches may liberate radiologists from time-consuming segmentation workloads and potentially make osteosarcoma radiomics an automatic pipeline for clinical use. In addition to segmentation, deep learning models have been compared with radiomics models and showed better performance in predicting NAC response and metastasis [41, 42], and the performance of radiomics models improved when incorporating deep learning features . The application of deep learning has not been detected by the previous review, but currently more studies used deep learning to further mine information in images. More studies tested their model using datasets from other institutions [33,34,35, 45] or splitting testing datasets [39, 44, 46,47,48, 50,51,52,53,54,55,56,57] to show the true performance of their models, while none of the studies in the previous review has been externally validated. The improvements in validation settings allow us to meta-analyze the performance of radiomics for prediction of NAC response based on testing datasets. The pooled DOR is lower than that in the previous review (28.83 vs 43.68), but result of the present review is more robust and interpretable . We only included MRI-driven radiomics models which have been evaluated on testing datasets [35, 39, 55, 57], while the previous meta-analysis was carried out based on any imaging modality or dataset.
Study quality has improved since the publication of the previous review. However, the overall study quality is suboptimal. RQS and TRIPOD have identified disadvantages in phantom study, cut-off analysis, cost-effectiveness analysis, blindness of assessment, sample size calculation, and missing data handling, which have been repeatedly addressed [8, 12,13,14]. The previous review only employed RQS for quality assessment. RQS was a specialized tool proposed to help the radiomics community assess the quality and value of a radiomics study. However, RQS was tailored on hand‐crafted features. As deep learning is gaining momentum, the current version of RQS may not capture the strengths and weaknesses of deep learning radiomics studies correctly . TRIPOD is a similar example that aimed to promote transparency reporting of diagnostic accuracy model studies and has been recommended to identify room for improvements in radiomics studies . Nevertheless, the current version of TRIPOD may not capture some unique challenges with machine learning or AI application . In contrast, CLAIM captured unique shortness in our review, such as data de-identification and failure analysis. CLAIM has been employed as a useful tool for quality evaluation in deep learning studies [20, 21], and our review demonstrated the feasibility of CLAIM in radiomics studies. We further confirmed that CLAIM can serve as a better review and study design guideline in radiomics studies. CLAIM may guide the update of TRIPOD and RQS, because it not only includes general reporting criteria, but also allows extra distinguishment of unique shortness in deep learning. CLAIM may even replace RQS and TRIPOD, considering the overlapping items and high correlation between these tools. The researchers are still reticent in publishing the RQS and TRIPOD for their radiomics studies . Only one study in our review included RQS, TRIPOD and CLAIM as supplementary materials .
Our review has several limitations. First, our review focused on osteosarcoma radiomics studies. The conclusion should be interpreted with caution when expanded to other diseases. However, it provided insights for the design and reporting radiomics studies. Second, our study only included AI research applying the radiomics approach, but overlooked those conducted with only deep learning for segmentation [60,61,62] or modeling . However, the secondary aim of our study is to find out whether CLAIM can better identify disadvantages in radiomics studies than the currently recommended RQS and TRIPOD. As CLAIM is suitable for both radiomics and deep learning radiomics studies, future review is encouraged to carry out without the restriction of radiomics. Third, it has not been investigated in our review how to weigh each item in CLAIM. The previous reviews have created subitems for some evaluations  and weighed them as equal . We treated each subitem as equal, but it is necessary to find out whether it is appropriate. Fourth, we did not employ more specific tools for evaluation, because they are not suitable or are currently under development [59, 64,65,66,67,68]. The review may benefit from the increasing study reporting guidelines for clinical studies using AI in healthcare, because they pay extra attention to additional factors which do not neatly conform to traditional reporting guidelines, especially details relating to technical algorithm development . The Image Biomarkers Standardization Initiative (IBSI) guideline is another potential eligible checklist for quality elevation . However, we did not apply it as previous reviews [14, 24], since this radiomics-specific checklist may not suitable for deep learning studies. Finally, due to the heterogeneity and limited numbers of studies, we only rated the evidence level of radiomics in prediction of NAC response. Further investigation is needed to lay a more robust scientific basis for translating the radiomics approach to a clinical useful tool [23, 24].
In conclusion, the quality of radiomics studies in osteosarcoma has improved in recent years, but is still suboptimal. MRI-driven radiomics for prediction of NAC response in osteosarcoma is rated as weak evidence according to meta-analysis of testing datasets, calling for more high-quality studies to promote radiomics application in osteosarcoma. CLAIM can better identify disadvantages in radiomics studies and therefore is recommended for future evaluation of AI studies including radiomics.
Availability of data and materials
All data generated or analyzed during this study are included in this published article and its supplementary information files.
Checklist for Artificial Intelligence in Medical Imaging
Diagnostic odds ratio
Modified Quality Assessment of Diagnostic Accuracy Studies
Radiomics Quality Score
Summary receiver operating characteristic
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The authors would like to express their gratitude to Dr. Jia Geng and Dr. Liping Si for their contribution on the previous version of this systematic review and meta-analysis; and Dr. Shiqi Mao for his suggestions on data visualization.
This study has received funding by Yangfan Project of Science and Technology Commission of Shanghai Municipality (22YF1442400); Shanghai Science and Technology Commission Science and Technology Innovation Action Clinical Innovation Field (18411953000); Medicine and Engineering Combination Project of Shanghai Jiao Tong University (YG2019ZDB09); and Research Fund of Tongren Hospital, Shanghai Jiao Tong University School of Medicine (TRKYRC-XX202204, 2020TRYJ(LB)06, 2020TRYJ(JC)07, TRGG202101, TRYJ2021JC06). They played no role in the study design, data collection or analysis, decision to publish, or manuscript preparation.
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. Note S1: Review protocol. Note S2: Search strategy and study selection. Note S3: Consensus reached during data extraction and quality assessment. Note S4: Data synthesis and analysis methods. Table S1: Data extraction sheet. Table S2: RQS elements according to six key domains. Table S3: TRIPOD reporting completeness checklist. Table S4: CLAIM for authors and reviewers. Table S5: QUADAS-2 tool for risk of bias and concern on application. Table S6: Category of five levels of supporting evidence of meta-analyzes. Table S7: Study characteristics of included studies. Table S8: PICOT of included studies. Table S9: Radiomics methodological issue of included studies. Table S10: Model presentation and performance metrics of included studies. Table S11: RQS rating per study. Table S12: TRIPOD adherence per study. Table S13: CLAIM adherence per study. Table S14: QUADAS-2 assessment per study. Table S15: Subgroup analysis of study quality according to study characteristics. Table S16: Model metrics of studies included in meta-analysis. Figure S1: Correlation between quality evaluation tools. Figure S2: Subgroup analysis of quality evaluation results. Figure S3: Forrest plot of pooled sensitivity. Figure S4: Forrest plot of pooled specificity. Figure S5: Forrest plot of pooled positive likelihood ratio. Figure S6: Forrest plot of pooled negative likelihood ratio. Figure S7: SROC curve of the model performance. Figure S8: Funnel plot of studies included in meta-analysis. Figure S9: Deeks' funnel plot of studies included in meta-analysis. Figure S10: Trim and fill analysis of studies included in meta-analysis.
. PRISMA 2020 checklist.
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Zhong, J., Hu, Y., Zhang, G. et al. An updated systematic review of radiomics in osteosarcoma: utilizing CLAIM to adapt the increasing trend of deep learning application in radiomics. Insights Imaging 13, 138 (2022). https://doi.org/10.1186/s13244-022-01277-6
- Machine learning
- Quality improvement
- Systematic review