Introduction

Thyroid disease is highly prevalent throughout the world [1, 2]. High-resolution ultrasound (US) is the first-line imaging examination modality for the thyroid disease [3, 4]. It can help to detect and manage thyroid nodules in combination with risk stratification systems, follow up the patients after thyroid cancer surgery [5, 6], and manage diffuse thyroid disease (DTD) by identifying changes in thyroid size and internal structure [7, 8].

Due to the imbalance of medical resources, professional health services are often lacking in rural and remote areas [9]. It forces patients to travel long distance to larger hospitals, which increases the economic cost of patients and the burden of larger hospitals [10]. A global study by Sina et al. showed that the quality of care for patients with thyroid cancer was poorer in low socio-economic areas than in high socio-economic areas [11]. Therefore, an effective method is needed to improve the diagnosis and management of thyroid disease for patients in rural and remote areas.

Telemedicine is recognized as a useful method to address the barriers in accessing to healthcare and medical resources through Internet communication technology. Many studies have proved that telemedicine can overcome the geographic restrictions, alleviate the contradiction between supply and demand, and effectively realize the reasonable distribution of quality medical services [12, 13]. Tele-ultrasound (Tele-US) is an important branch of telemedicine [14, 15]. Thomas et al. used asynchronous mode to transmit thyroid US images and dynamic videos of Peruvian patients for expert interpretation [15]. However, the acquisition and interpretation of dynamic US is highly operator dependent, which might result in different management options [16].

With the advancement of communication technology, robot arm control and computer technology, telerobotic US could be used as a reliable solution to achieve cross-regional sharing of medical resources [17]. Experienced doctors can examine patients remotely by manipulating robotic arm to enable patients to access individualized medical services locally. Previous studies found that telerobotic US had achieved promising results in the abdomen, obstetrics, echocardiograph, vascular examinations, and intensive care unit [18,19,20,21,22,23].

The application of state-of-the-art 5th generation (5G) mobile communication technology and telerobotic US technology has potential to provide effective thyroid examination and patient management in remote areas with limited medical resources, especially during the COVID-19 pandemic. Therefore, this study prospectively evaluated the clinical feasibility and accuracy of 5G-based telerobotic US for thyroid examination on a rural island.

Materials and methods

This prospective study followed the principles of the Declaration of Helsinki and was approved by the Ethics Committee of the Shanghai Tenth People’s Hospital (approval number: SHSY-IEC-4.1/21-261/01). Informed consent was obtained from all participating patients. This clinical trial was registered at www.chictr.org.cn (ChiCTR2200055337).

Study participants

From September 2020 to March 2021, 148 consecutive patients were referred to Chongming Second People’s Hospital, Chongming Island, China, for thyroid US examinations. Chongming Second People’s Hospital is 72 km away from Shanghai Tenth People’s Hospital, which is a tertiary referral center. The inclusion criteria for patients were as follows: (a) Age ≥18 years and ≤80 years; (b) Agreed to participate in the trial. The exclusion criteria were as follows: (a) Robotic arm failure of telerobotic US (n = 2); (b) Incomplete US imaging data (n = 7). Finally, a total of 139 patients who underwent both conventional thyroid US and 5G-based telerobotic thyroid US examinations were recruited in this study.

5G-based telerobotic US system

The 5G-based telerobotic US system (MGIUS-R3, MGI Tech Co., Ltd., Shenzhen, China) consists of a doctor’s subsystem and a patient’s subsystem. Two subsystems are connected by the fast and large-bandwidth 5G network. The 5G network system enables real-time transmission of US and audio-visual data between the doctor’ subsystem and the patient’ subsystem, with a download rate of about 930 Mbps and an upload rate of about 130 Mbps. There is no significant delay in the examination process (≤200 ms).

The doctor’s subsystem is equipped with the robot control console, the US system control platform, and the audio-visual communication system. It was located at the Shanghai Tenth People’s Hospital. The robot control console of doctor-side subsystem consists of a mobile mock US probe, a built-in position sensor, and a built-in pressure sensor. The mock US probe is equipped with a gesture sensor and a “UP” button. By associating the robot control console coordinate system with the robot coordinate system, the robot control console is able to manage six DOFs of robotic arm. As a result, the action of the operator is consistent with the action of the robotic arm. The gesture sensor manages three DOFs for rotation, the position sensor manages two DOFs for the movement on the horizontal plane, the “UP” button and pressure sensor manage one DOF for the up and down movement, respectively [29], which can show how the operator can make better decision when they are deprived of relevant information. Thus, additional investigations based on force sensing might also help overcome the occurrence of uncomfortable conditions in patients.

The limitations of the network made the image quality less clear, which to some extent affected the diagnostic effectiveness and clinical application of telerobotic US [18, 30]. Arbeille et al. used telerobotic US to examine the abdomen at low bandwidth network, and the degradation of US images quality resulted in 6 (17%) cases of unvisualized lesions [18]. As a new generation of mobile communication technology with high speed, wide spectrum, and low latency, 5G effectively overcomes the impact of previous low bandwidth on US image transmission. Our study indicated that the quality of 5G-based telerobotic US images was comparable to that of conventional US, meeting the diagnostic requirements of tele-doctors. Compared with 4G network, its transmission rate is increased by 10–100 times, the peak value can reach 10 Gb/s, and the time delay is reduced by about 9/10, reaching the millisecond level, which is conducive to acquisition, transmission, analysis, and processing of original US images and accurate synchronization of various audio-visual information over long distances. Furthermore, 10% of patients felt tension and fear when the robotic arm was moving. The adequate information prior to examination and communication between the tele-doctors and the patients during examination are necessary.

The use of telerobotic technology focusing on thyroid examination has been reported in the several previous studies [19, 31,32,33]. Georgescu et al. from a French group performed 33 thyroid telerobotic US examinations using the Melody system [19]. However, this study was case series with no comparison to a reference standard for assessment of diagnostic accuracy and the potential of the system to identify thyroid disease has also not been evaluated in detail. Kojcev et al. proposed a robotic framework and found that robotic US enables more repeatable thyroid measurements in four healthy volunteers as compared to the expert [32]. Similar, a study by Kaminski et al. utilized a seven-axis robotic arm capable of 6-DoF force-torque sensing can acquire repeatable automatic thyroid US scanning with the combination of predefined trajectory execution and real-time force feedback control on a tissue-mimicking phantom containing thyroid features [33]. Nevertheless, these robotic US platforms are still experimental and not yet commercially available. To the best of our knowledge, this is the first prospective and cross-sectional study that perform a comprehensive assessment of the clinical use of 5G-based telerobotic US in thyroid disease in comparison to conventional US.

In this study, 20 patients had DTD, of which 15 patients had asymptomatic health check and 5 patients had neck discomfort. The results of 5G-based telerobotic US diagnosis were consistent with those of conventional US diagnosis. Combined with clinical laboratory indicators, the accuracy of telerobotic US in identifying subclinical DTD was 94.4%. This result suggested that telerobotic US may be a useful diagnostic tool to detect DTD in clinical practice. Furthermore, US diagnostic information can be delivered to the patient’s side endocrinologist to receive timely administration of medication or other relevant treatments. DTD includes thyroiditis (mainly Hashimoto’s thyroiditis and Graves’ disease) and goiter [34]. Previous studies have reported that approximately 20% Graves’ disease and more than 90% Hashimoto’s thyroiditis are subclinical and is associated with increased risk of cardiovascular disease and mortality [35, 36]. Subclinical disease also make assessment more difficult [7, 37], but US can identify this subset of patients before they come to clinical attention by monitoring abnormal echogenicity and size changes [34]. Current literature indicated that the specificity and sensitivity of US in determining subclinical cases of DTD were 92.1% and 87.7%, respectively [8].

Inspection of cervical lymph nodes is a key step of thyroid examination. Identification of abnormal cervical lymph nodes contributes to stratify the risk of suspected thyroid nodules and make treatment planning for thyroid cancers [38]. For patients with thyroid cancer after surgery, cervical US to evaluate the thyroid bed and central and lateral cervical nodal compartments should be performed at 6–12 months. US can predict lymph node abnormalities by detecting suspicious features such as long-to-short-axis ratio < 2, hyperechogenic hilum, microcalcification, cystic change, and peripheral vascularization [39, 40]. Of these features, microcalcifications and cystic change have been shown to have the highest specificity (up to 100%), whereas peripheral vascularization has the highest combined sensitivity and specificity (86% and 82%) [40]. Overall good results of the cervical lymph nodes examination have been achieved in our study. It should be noted that telerobotic US examination was also challenging when swee** the lymph nodes in the cervical V region, because this region is a convex lateral zone and the robotic arm has restrictions on the side through the supine position. Consequently, the patient’s body position needs to be tilted to the other side to achieve the desired orientation required for the examination.

There were no major differences between the parameters measured by the two methods. Similarly, the images allowed 96.6% of abnormalities to be detected, indicating a high diagnostic performance during telerobotic US. However, five thyroid nodules were missed, which may be attributed to poor contact between the US transducer and the skin adjacent to the trachea. In addition, two patients had heterogeneous thyroid background which interfered with the diagnosis of thyroid nodules. Besides, the missed thyroid nodules of both telerobotic US and conventional US indicated the dependence of the US operator. The most US features of the same thyroid nodules obtained from the telerobotic US examination were in good agreement with the conventional US examination. Besides, the relatively lower metric obtained for margins in this study might be due to the intrinsic difficulty in assessing this feature.

The 5G-based telerobotic US examinations could make a difference in clinical practice, widening health coverage and reducing the associated costs. Beyond that, when storing the US image, the picture of the overall external environment of the US transducer’s position was also stored. It is beneficial not only to the location of thyroid nodules but also to follow-up examinations. Moreover, during the examination, both the static US images and the dynamic videos were stored, which was conducive to repeated dynamic assessment. Furthermore, the telerobotic US system can scan the patient’s lateral cervical region. An ergonomic arm cushion was equipped next to the operation panel, and tele-doctors could place their arm on the cushion during the US examination to relieve arm fatigue and reduce chronic musculoskeletal injuries.

There were some limitations in this study. First, it was a single-center study with relatively small samples. We will cooperate with multiple centers to obtain more sample data to further validate the value of the 5G-based telerobotic US for thyroid evaluation in the future. Second, the verification of pathological results of thyroid nodules was lacking, which may affect the generality of our findings and the accuracy of diagnosis to a certain extent. Third, the fixed camera was located on the right side of the patient in current telerobotic US system, and the tele-doctors cannot clearly monitor the position of the US transducer on the left side of the neck. Thus, it is necessary to increase the number of cameras so that the doctor’ side can clearly visualize the left side of the patient’s neck. Finally, the on-site assistant was involved for ensuring continuity and efficiency of the telerobotic US examination in this study. In order to improving up this telerobotic US system to become feasible even when the on-site assistant is not available, further efforts are needed like endowing the operational site with suitable visual sensors and installing the equipment that can remotely control the application of US coupling agent.

This study provided robust evidence that 5G-based telerobotic US is feasible, which can provide qualified thyroid examination to help patients with thyroid diseases on a rural island. It can achieve the same effect as face-to-face and close-range conventional US examination without reducing diagnostic accuracy or increasing related procedural times.