Abstract
Artificial intelligence (AI)-based radiomics has attracted considerable research attention in the field of medical imaging, including ultrasound diagnosis. Ultrasound imaging has unique advantages such as high temporal resolution, low cost, and no radiation exposure. This renders it a preferred imaging modality for several clinical scenarios. This review includes a detailed introduction to imaging modalities, including Brightness-mode ultrasound, color Doppler flow imaging, ultrasound elastography, contrast-enhanced ultrasound, and multi-modal fusion analysis. It provides an overview of the current status and prospects of AI-based radiomics in ultrasound diagnosis, highlighting the application of AI-based radiomics to static ultrasound images, dynamic ultrasound videos, and multi-modal ultrasound fusion analysis.
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Introduction
Ultrasound has become an indispensable tool for medical diagnosis and treatment because of its non-invasiveness, portability, and real-time imaging capabilities [1]. Artificial intelligence (AI)-based radiomics, the use of machine learning algorithms to extract and analyze quantitative features (such as texture, shape, and intensity) from medical images to assist clinicians to diagnose and predict disease prognosis, has attracted research attention in the field of medical imaging, including ultrasound diagnosis [2,3,4]. It has been extensively studied using various medical imaging modalities, including computed tomography (CT), magnetic resonance imaging (MRI), and positron emission tomography [5,6,7,8,9,10,11,12,13]. However, compared to other imaging modalities, ultrasound imaging has unique advantages such as high temporal resolution, inexpensiveness, and no radiation exposure. This renders it a preferred imaging modality for several clinical scenarios [14]. The application of AI-based radiomics in ultrasound diagnosis has attracted increasing attention from researchers and clinicians recently.
This review includes a detailed introduction to imaging modalities, including B-mode ultrasound (BUS) [15], color Doppler flow imaging (CDFI) [16], ultrasound elastography (UE) [17], contrast-enhanced ultrasound (CEUS) [18], and multi-modal fusion analysis of BUS, CDFI, UE, and CEUS. It aims to provide an overview of the current status and prospects of AI-based radiomics in ultrasound diagnosis by highlighting the application of AI-based radiomics to static ultrasound images, dynamic ultrasound videos, multi-modal ultrasound fusion analysis, and advanced methods of intelligent ultrasound analysis.
AI has three fundamental tasks in the field of ultrasound: classification, segmentation, and detection. Static ultrasound involves two-dimensional imaging. Furthermore, BUS images reflect the anatomical structure of lesions and are commonly used for classification and segmentation tasks. Additionally, CDFI images reflect the blood flow information of lesions, whereas UE images reflect the tissue hardness of lesions. These two modalities are often used for classification tasks. Dynamic ultrasound involving videos (BUS videos) dynamically reflect changes in the anatomical structure and position of lesions and are frequently used for tasks such as classification, segmentation, detection, and tracking. In addition, CEUS reflects dynamic changes in blood flow and is commonly used for classification. The relationships between AI tasks and different ultrasound modalities are shown in Table 1.
In the next few sections, the applications of AI in ultrasound diagnosis will be discussed in detail. In the static ultrasound image section, the application of AI-based radiomics to extract quantitative features (such as tumor size, shape, texture, and echogenicity) from ultrasound images to assist in the diagnosis and differentiation of various diseases is discussed. The application of AI-based radiomics to analyze changes in the intensity and texture of lesions during the CEUS process is introduced in the dynamic ultrasound video section. This can provide valuable information for the diagnosis and treatment of diseases.
In the multi-modal ultrasound fusion analysis section, the use of AI-based radiomics to integrate information from multiple ultrasound modalities, such as BUS, CDFI, UE, and CEUS, and improve the accuracy of disease diagnosis and treatment planning is discussed. Tables 2, 3 and 4 present the related studies, their aims, and the performance of the AI algorithms, respectively. In addition, the challenges and limitations of AI-based radiomics in ultrasound diagnosis, such as the lack of standardization in feature extraction and the need for large-scale multicenter studies to validate the clinical efficacy of AI-based radiomics is discussed.
AI-based radiomics has the potential to revolutionize the field of ultrasound diagnosis by providing objective and quantitative analyses of ultrasound images. This can improve the accuracy and efficiency of disease diagnosis and treatment. This review provides valuable insights into the current status and future prospects of AI-based radiomics in ultrasound diagnosis and serves as a useful reference for researchers and clinicians in this field.
Application of AI-based radiomics in ultrasound diagnosis
Static ultrasound
Static ultrasound refers to the use of BUS, color CDFI, and UE to generate static images of tissues and organs within the body. These modalities are widely used in medical diagnosis and research, and they provide valuable information on the morphology, vascularity, and elasticity of various tissues. Static ultrasound imaging modalities provide detailed spatial information about tissues and organs, rendering them valuable tools for medical diagnosis and research. Owing to the advancement in technology and an increased understanding of its clinical utility, static ultrasound plays an important role in AI-based radiomics in ultrasound diagnosis (Fig. 1).
BUS
This is the most common type of ultrasonography and involves various examinations. Analysis of ultrasound images performed using AI differs for different examination sites and purposes. It mainly performs classification, segmentation, and detection tasks.
The most common classification task is diagnostics. Specifically, there are diagnoses of specific diseases by traditional and deep learning, such as diagnosis of hepatocellular carcinoma (HCC) [50], triple negative breast cancer [19], cervical tuberculous lymphadenitis [51], and v-raf murine sarcoma viral oncogene homolog B (BRAF) mutation in thyroid cancer [52]. These are generally dichotomous tasks (diagnosis as positive or negative) and staging of the same lesion (such as liver fibrosis staging [41], lung B-line severity assessment [53], classification of COVID-19 markers [54], and determination of the type of liver lesion [55]). They are generally multi-classified tasks. Additional categorical tasks include the preoperative prediction of Ki-67 expression levels in breast cancer patients [56], prediction of axillary lymph node metastasis in breast cancer patients [20], and distant metastasis in follicular thyroid cancer [21]. The classification task usually extracts the features of BUS images from the region of interest (ROI) selected by the doctor. Some of them add relevant data features and use them to make judgments. Some of the tasks generate heat maps by the AI after the judgment, which explains the AI’s judgment and inspires the doctors to summarize their experiences. A heatmap is an image that describes which regions of an input image a model focuses on. The colors’ intensity in the heatmap indicates the level of attention the model gives to corresponding areas. Doctors can use heatmaps to understand which regions the model prioritizes. This enables targeted observation and study of those specific areas, leading to the accumulation of experience for diagnosis and prognosis prediction.
The classification task makes a judgment on the entire image, whereas the detection task adds a localization task to the judgment. This can localize the carotid artery cross-section in ultrasound images [57], lesions on abdominal ultrasound images [58], and thyroid nodules [59]. The detection task can generate multiple labels on a single BUS image. It uses rectangular boxes to mark the positions corresponding to the labels and can handle multiple ROIs in a single image.
The segmentation task is a more accurate classification task. It classifies each pixel point, after which information such as the boundary, size, and location of different regions in the ultrasound image becomes clear. AI can perform arterial plaque [22, 60, 61], breast tumor [23] proposed the use of a newly developed deep learning radiomics of elastography (DLRE) model to assess liver fibrosis stages. DLRE adopts a radiomic strategy for the quantitative analysis of heterogeneity in two-dimensional shear wave elastography (SWE) images. This study aimed to address the clinical problem of accurately diagnosing the stages of liver fibrosis in hepatitis B virus-infected patients using noninvasive methods, a significant challenge for conventional approaches. Zhou et al. [26] proposed deep learning radiomics of an elastography model, which adopted a CNN based on transfer learning as a noninvasive method to assess liver fibrosis stages. This is essential for the prognosis and surveillance of chronic hepatitis B patients. Lu et al. [25] proposed an updated deep-learning radiomics model of elastography (DLRE2.0) to discriminate significant fibrosis (≥ F2) in patients with chronic liver disease. The dataset used in their study included 807 patients and 4842 images from three hospitals. The DLRE2.0 model showed a significantly improved performance compared to the previous DLRE model with an AUC of 0.91 for evaluating ≥ F2. The radiomics models showed good robustness in an independent external test cohort. Destrempes et al. [84] proposed a machine learning model based on random forests to select combinations of quantitative ultrasound features and SWE stiffness for the classification of steatosis grade, inflammation grade, and fibrosis stage in patients with chronic liver disease.
The UE-based AI can also improve the classification and diagnosis of lymph diseases. Zhang et al. [85] used a random forest model for the differential diagnosis of thyroid nodules based on conventional ultrasound and real-time UE. Qin et al. [86] proposed a method based on a CNN that combined the characteristics of conventional ultrasound and ultrasound elasticity images to form a hybrid feature space for the classification of benign and malignant thyroid nodules. Zhao et al. [87] used a machine learning model that incorporated radiomic features extracted from ultrasound and SWE images to develop ML-assisted radiomics approaches. Liu et al. [88] proposed a radiomic approach using BUS and strain elastography to estimate the lymph node status in patients with papillary thyroid carcinoma.
UE is an adjunctive instrument for refining the identification and non-intrusive delineation of breast lesions, facilitating radiologists in amplifying patient care. The incorporation of SWE into BUS demonstrated the potential to provide supplementary diagnostic insights and to reduce the need for unwarranted biopsies [89]. Li et al. [90] proposed an innovative dual-mode AI architecture that could automatically integrate information from ultrasonography and SWE to assist in breast tumor classification. Kim et al. [91] used deep learning-based computer-aided diagnosis and SWE with BUS to evaluate breast masses detected by screening ultrasound and addressed the low specificity and operator dependency of breast ultrasound screening.
Similarly, UE is also widely used to diagnose other diseases. Additionally, UE-based AI can improve lymph node classification, compared to that performed only by radiologist evaluations. Tahmasebi et al. [24] evaluated an AI system for the classification of axillary lymph nodes on UE. They aimed to compare the performance of the AI system with that of experienced radiologists in predicting the presence of metastasis to the axillary lymph nodes on ultrasound.
AI + UE has shown considerable potential in revolutionizing medical diagnoses. It offers a partial solution to the limitations of UE, enhances diagnostic accuracy, and enables individualized classification and predictive models for liver diseases. Additionally, UE-based AI can aid in lymph node disease classification and non-intrusive delineation of breast lesions, reducing the need for unnecessary biopsies and improving patient care. Furthermore, the application of AI to other diseases (such as lymph node classification) highlights its ability to outperform radiologist evaluations. The combination of AI and UE can advance medical imaging and patient outcomes.
Waveform graph
Doppler ultrasound is capable of measuring blood flow velocity, which results in a waveform graph showing the blood supply. No prior studies were found for the use of AI to analyze Doppler flow spectrograms. However, a study conducted to diagnose early allograft dysfunction in liver transplant patients showed that a deep learning model could be used to analyze and determine blood flow spectrograms. The results of the AI analysis of the flow velocity spectrograms related to blood flow can lead to medical conclusions related to blood flow, such as determining the cause of the disease to assist the physician’s treatment. Because the results learned by AI are significantly better than the empirical results of doctors, the heat maps generated assist doctors to understand the information contained in blood flow spectrograms.
Dynamic ultrasound
Dynamic ultrasound (also known as CEUS) is an effective imaging tool for analyzing the spatiotemporal characteristics of lesions and diagnosing or predicting diseases. Real-time high-resolution images produced by CEUS are often comparable to those obtained by CT or MRI [92]. Thus, a quick, reliable, and relatively inexpensive CEUS may reduce the need for additional testing. Additionally, CEUS is routinely used worldwide to detect heart disease and stratify the risk of heart attack or stroke. It is also used to identify, characterize, and stage tumors of the liver [93], kidney [94], prostate [95], breast [96], and other organ systems and to monitor the effectiveness of cancer therapies. However, because CEUS is considerably affected by operator bias, the image quality is relatively unstable and the tumor boundary (TB) is often unclear. These disadvantages often limit the accuracy of the direct analysis by radiologists. Therefore, several studies recently tend to use deep learning methods to extract spatiotemporal features from CEUS sequences to assist treatment (Fig. 2).
Furthermore, AI deep-learning models can aid in diagnostic classification. Tong et al. [27] developed an end-to-end DLR model based on CEUS to assist radiologists in identifying pancreatic ductal adenocarcinoma and chronic pancreatitis. To train and test the model, 558 patients with pancreatic lesions were included. The DLR model achieved an AUC of 0.986 (95%CI: 0.975–0.994), 0.978 (95%CI: 0.950–0.996), 0.967 (95%CI: 0.917–1.000), and 0.953 (95%CI: 0.877–1.000) in the training, internal validation, and external validation cohorts 1 and 2, respectively. Similarly, Chen et al. [28] proposed a three-dimensional CNN model based on CEUS videos. This model was validated using a Breast-CEUS dataset comprising 221 cases. The results show that the proposed model in this study achieved a sensitivity and an accuracy of 97.2% and 86.3%, respectively. The incorporation of domain knowledge led to a 3.5% and 6.0% improvement in sensitivity and specificity, respectively. Liu et al. [29] established and validated an AI-based radiomics strategy for predicting personalized responses of patients with HCC to the first transarterial chemoembolization (TACE) session by quantitatively analyzing CEUS cines. One hundred and thirty patients with HCC (89 and 41 for training and validation, respectively) who underwent ultrasound examinations (CEUS and BUS) within one week before the first TACE session were retrospectively enrolled. The AUCs of deep learning radiomics-based CEUS model (R-DLCEUS), machine learning R-TIC, and machine learning radiomics-based BUS images model were 0.93 (95%CI: 0.80–0.98), 0.80 (95% CI:, 0.64–0.90), and 0.81 (95%CI: 0.67–0.95) in the validation cohort, respectively.
In addition, AI deep learning algorithms can be used to select and predict treatment methods and effects, respectively. Liu et al. evaluated the performance of a deep learning-based radiomics strategy designed for analyzing CEUS to predict the progression-free survival (PFS) of radiofrequency ablation (RFA) and surgical resection (SR) and to optimize the treatment selection for patients with very early or early stage HCC [30]. Their study retrospectively enrolled 419 patients examined using CEUS within one week before receiving RFA or SR (RFA: 214, SR: 205) between January 2008 and 2016. The R-RFA and SR showed remarkable discrimination (C-index: 0.726 and 0.741 for RFA and SR, respectively). The model identified that 17.3% and 27.3% of the RFA and SR patients should swap their treatment, indicating that their average probability of two-year PFS would increase by 12% and 15%, respectively. Similarly, Sun and Lu [31] evaluated the efficacy of atorvastatin in the treatment of diabetic patients using CEUS, based on a three-dimensional reconstruction algorithm. One hundred and fifty-six DN patients were divided into experimental (conventional treatment + atorvastatin) and control (conventional treatment) groups. The kidney volume and hemodynamic parameters, including the maximal kidney volume, minimal kidney volume, and resistance index of all patients were measured and recorded before and after treatment. The volume (136.07 ± 22.16 cm3) in the experimental group after the treatment was smaller, in contrast to the control group (159.11 ± 31.79 cm3) (P < 0.05).
Because delineating the ROI containing the lesion and the surrounding microvasculature frame-by-frame in CEUS is a time-consuming task [32], some AI methods have been proposed to realize automatic segmentation of lesions. Meng et al. [32] proposed a novel U-net-like network with dual top-down branches and residual connections known as CEUSegNet. The CEUSegNet uses the US and CEUS parts of a dual-amplitude CEUS image as inputs. The lesion position can be determined exactly under US guidance, and the ROI can be delineated in the CEUS image. Regarding the CMLN dataset, CEUSegNet achieved 91.05% Dice and 80.06% intersection over the union (IOU). Considering the BL dataset, CEUSegNet achieved 89.97% Dice and 75.62% IOU. Iwasa et al. [33] evaluated the capability of the deep learning model U-Net for automatic segmentation of pancreatic tumors on CEUS video images and the possible factors affecting automatic segmentation. This retrospective study included 100 patients who underwent CEUS for pancreatic tumors. The degree of respiratory movement and TB were divided into three-degree intervals for each patient and were evaluated as possible factors affecting the segmentation. The concordance rate was calculated using IOU. The median IOU for all the cases was 0.77. The median IOU for TB-1 (approximately clear), TB-2, and TB-3 (more than half unclear) were 0.80, 0.76, and 0.69, respectively. The IOU of TB-1 was significantly higher than that of TB-3 (P < 0.01).
Thus, CEUS is a powerful tool for diagnosing and predicting various diseases. It offers real-time high-resolution images comparable to those of CT or MRI, thereby reducing the need for additional tests. Although AI-based deep learning models are affected by operator variability and unclear tumor boundaries, they can assist radiologists in obtaining precise diagnosis and treatment selection. Furthermore, AI models have achieved impressive results in classifying pancreatic lesions, predicting liver fibrosis stages, and optimizing the treatment choices for patients with HCC. Additionally, AI can aid in lesion segmentation, automate time-consuming processes, and improve accuracy. Integrating AI with CEUS has immense potential for advancing medical imaging and improving patient outcomes.
Dual-/multi-modal ultrasound and AI-powered ultrasound image analysis
Various ultrasound modalities depict lesions from different aspects, which provides clinicians with the power to understand lesions more comprehensively. Naturally, a more satisfactory performance is expected via intelligent fusion analysis of combinations of ultrasound modalities. Existing studies in the area of dual/multi-modal ultrasound fusion analysis can be divided into two parts: clinical application and algorithm studies, which focus on the performance of specific clinical problems and the development of fusion methods. Figure 3 summarizes the related studies in recent years.
Conclusions
Ultrasound diagnosis is widely used in clinical practice because of its noninvasive and real-time imaging capabilities. Radiomics, an emerging field in medical imaging, can extract quantitative features from medical images and provide a comprehensive analysis of image data. The application of AI in radiomics has significantly improved the accuracy and efficiency of ultrasound diagnosis. Static ultrasound images such as BUS, CDFI, and UE are widely used in clinical practice. Additionally, AI-based radiomics can analyze the texture, shape, and other quantitative features of images to identify patterns and provide diagnostic information. For example, AI-based radiomics have been used to differentiate benign from malignant thyroid nodules using BUS images with high accuracy. Dynamic ultrasound videos such as CEUS, provide additional information on the blood flow and perfusion of the imaged tissue. Additionally, AI-based radiomics can be used to analyze temporal changes in contrast enhancement and provide a more accurate diagnosis of liver tumors, breast lesions, and other diseases. Multi-modal ultrasound fusion analysis combines multiple ultrasound imaging modalities (such as BUS, CDFI, UE, and CEUS) to provide a comprehensive analysis of the imaged tissue. Furthermore, AI-based radiomics can be used to analyze the quantitative features of these images to provide a more accurate and comprehensive diagnosis. For example, AI-based radiomics has been utilized to differentiate malignant and benign breast lesions using a combination of BUS, CDFI, and CEUS images. In conclusion, AI-based radiomics has a considerable potential for improving the accuracy and efficiency of ultrasound diagnoses. By analyzing the quantitative features of static ultrasound images, dynamic ultrasound videos, and multi-modal ultrasound fusion, AI-based radiomics can provide a more accurate diagnosis of various diseases (including liver tumors, breast lesions, and thyroid nodules). However, some challenges (such as the need for large-scale datasets and standardized imaging protocols) must be addressed. With further research and development, AI-based radiomics are expected to play an increasingly important role in ultrasound diagnosis.
Availability of data and materials
Not applicable.
Abbreviations
- B-mode:
-
Brightness-mode
- AI:
-
Artificial intelligence
- CT:
-
Computed tomography
- MRI:
-
Magnetic resonance imaging
- BUS:
-
B-mode ultrasound
- CDFI:
-
Color doppler flow imaging
- UE:
-
Ultrasound elastography
- CEUS:
-
Contrast-enhanced ultrasound
- ROI:
-
Region of interest
- CNN:
-
Convolutional neural network
- DLRE:
-
Deep learning radiomics of elastography
- SWE:
-
Shear wave elastography
- HCC:
-
Hepatocellular carcinoma
- TACE:
-
Transarterial chemoembolization
- R-DLCEUS:
-
Radiomics-based CEUS model
- R-TIC:
-
Radiomics-based time intensity curve of the CEUS model
- R-BMode:
-
Radiomics-based BUS image model
- PFS:
-
Progression-free survival
- RFA:
-
Radiofrequency ablation
- SR:
-
Surgical resection
- IOU:
-
Intersection over union
- TB:
-
Tumor boundary
- AGI:
-
Artificial general intelligence
- DLR:
-
Deep learning radiomics
- SVM:
-
Support vector machine
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This study was supported by the National Natural Science Foundation of China, Nos. 92159305, 92259303, 62027901, 81930053, and 82272029; Bei**g Science Fund for Distinguished Young Scholars, No. JQ22013; and Excellent Member Project of the Youth Innovation Promotion Association CAS, No. 2016124.
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HYZ designed the study and completed the final manuscript; ZLM wrote the dual-/multimodal ultrasound and AI-powered ultrasound image analysis; JYR wrote the dynamic ultrasound; YQM wrote the BUS; and KW supervised the study. All the authors have read and approved the final manuscript.
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Zhang, H., Meng, Z., Ru, J. et al. Application and prospects of AI-based radiomics in ultrasound diagnosis. Vis. Comput. Ind. Biomed. Art 6, 20 (2023). https://doi.org/10.1186/s42492-023-00147-2
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DOI: https://doi.org/10.1186/s42492-023-00147-2