Imaging the fine-meshed network of the lymphatic system has remained a major challenge, as it is difficult to access with various contrast agents, unlike the usual contrast examinations performed in the radiology department. An accurate and sensitive imaging technique is required to visualize the lymph vessels and flow to identify abnormalities such as lymphedema and lymphangiectasia. This is necessary to obtain a correct diagnosis and create a patient-specific therapy plan. Over the years, several imaging techniques have emerged to enable the visualization of the peripheral lymph vessels and their flow, each with its own advantages and limitations.

Lymphangiography of the extremities can be performed by injecting ethiodized oil as a contrast agent, either inter-digitally or directly into a lymph vessel in the foot. In lymphoscintigraphy, a radioactive agent (^99mtechnetium nano-colloid) is injected inter-digitally and its path is then followed through the extremities, with the resulting images being low-resolution. Alternatively, the superficial (peripheral) lymphatic vessels can be visualized using indocyanine green; however, this is a time-consuming technique that also results in low-resolution images. Other radiological modalities, such as magnetic resonance imaging, computed tomography, and fluoroscopy [1,2], can be used for lymphangiography after a minimally invasive inguinal intranodal contrast injection, enabling the visualization of the central, para-aortoiliac lymphatic vessels. This can be of diagnostic relevance in cases of chylothorax or chylous ascites [3,4]. These methods are all laborious and time-consuming.

In search of a more easily applicable, high-resolution, and dynamic modality, state-of-the-art ultrasound techniques could be applied to image superficial lymphatic vessels. These techniques have also been able to provide slow-flow information. The use of contrast-enhanced ultrasonography (CEUS) with an intranodal injection of microbubbles (Sonovue, Bracco, Milan, Italy), has proven valuable for imaging both central [5] and peripheral lymphatic vessels [6,7]. Dynamic imaging gives insights into the flow direction, which can be normal antegrade, abnormally retrograde, or both. Furthermore, several ultrasound manufacturers have recently developed microvascular flow imaging (MVFI) techniques (e.g., Superb Microvascular Imaging [SMI] by Canon Medical Systems, Tokyo, Japan; Micro Flow Imaging by Philips Medical Systems, Best, The Netherlands; Slow Flow by Siemens Healthineers, Erlangen, Germany; Microvascular Imaging by GE Healthcare, Chalfont St Giles, UK; and MV-flow by Samsung Healthcare, Seoul, Korea). These techniques use different algorithms from the conventional Doppler techniques, in order to visualize slow-flow velocity and small-diameter (blood) vessel flow. MVFI could play a role in the niche where CEUS is used [8]. Some studies have even suggested that MVFI is a valuable alternative to CEUS [9,10].

Due to the improved resolution of ultrasound machines and their potential to image low-flow velocities, the combination of high-resolution ultrasonography (HR-US) and MVFI could be applied to the imaging of vessels that transport fluids at very slow rates. The authors have started to explore the potential of using HR-US and MVFI in imaging the superficial lymphatic vessels. This technical note presents the first results.

The main finding of this study is that HR-US seems to be a valuable method for visualizing the superficial lymphatic vessels and flow. It was possible to distinguish normal antegrade from abnormal and retrograde flow, as well as normal from ectatic lymph vessels.

Until recently, conventional B-mode ultrasound techniques were not suitable for imaging small lymphatic vessels or measuring very slow lymphatic flow. However, recent technical advances have made ultrasonography a potential lymphatic imaging modality due to major improvements in temporal and spatial resolution, leading to the development of HR-US. Previously, HR-US using transmitted frequencies above 15 MHz, was only feasible using specialized, pre-clinical imaging systems [12]. Recent developments in transducer technology have produced a clinical transducer operating up to 29 MHz, resulting in HR-US images with an extremely high resolution of 70 μm [13]. Conventional color Doppler flow imaging (CDFI) uses a filter to remove motion, clutter, and wall artifacts, but low-flow information is removed as well. The algorithm of MVFI analyzes clutter not only in the temporal domain, but also in the spatial domain. This results in improved removal of the wall and motion artifacts, while preserving low-flow information. Consequently, MVFI provides images with very slow flow, down to 0.3 cm/s (0.3 cm/s is the lowest velocity that can be utilized on the scale of SMI. No documentation regarding minimal flow velocity is available at this moment).

Imaging of the lymphatic vessels has always been a challenge [4], and each imaging method has its disadvantages, such as being laborious or having low temporal or spatial resolution. In search for a more easily applicable imaging modality, HR-US with MVFI has potential as a relatively inexpensive, dynamic, and fairly quick technique to image superficial lymphatic vessels. MVFI has the advantage of high frame rates, high sensitivity, and—due to its algorithm—a reduced presence of artifacts, potentially making it a feasible technique for detecting slow superficial lymphatic flow [14,15]. The mSMI mode improves flow sensitivity by subtracting the background information from grayscale images and focusing only on the flow in the vessels [8]. SMI has been studied for use in the detection of sentinel lymph nodes and micro-vascularization in superficial tissues and organs, providing additional information in ultrasound examinations [9,14]. The advantage of SMI over CDFI is that with SMI, most of the hindering motion artifacts are removed, thus revealing the true flow [15,16]. The patency of thoracic duct outflow has been studied using CEUS [17]. Previous studies have investigated the applicability of MVFI in characterizing thyroid lesions [16,18,19] and renal masses [10] in comparison to CEUS. Some studies have compared the efficacy of both CEUS and MVFI for various applications [10], suggesting that MVFI is a valuable alternative for CEUS [9,10] or may even function as a replacement for CEUS in certain cases [8,18]. With the intranodal technique, imaging is limited to only the locoregional area of interest, due to the fact that the lymphatic flow is visualized using the pressure applied using the syringe. Malposition of the intranodal needle can lead to venous outflow after the injection of saline. This may be seen as diluted and relatively fast outflow. The venous vessels are larger than the lymph vessels and will possibly show a lower intensity in the mSMI-box due to the dilution of the flow within the slow bloodstream. Lympho-venous shunting is expected to show similar venous flow, but this possibility requires further investigation.

Smooth muscle cells in the lymphatic wall, adjacent muscle contractions, arterial flow, and respiratory movements of the chest cavity all contribute to antegrade lymphatic flow [11]. This study found that in cases of high systemic (iatrogenic or traumatic) lymphatic pressure, lymphedema, or abnormal anatomy, MVFI can be used to determine retrograde flow or local flow into the dermal layers. In line with previous studies that assessed other body parts, HR-US and MVFI were found to be useful additional tools for imaging superficial lymphatic vessels. Further investigations could determine whether HR-US and MVFI are feasible in diagnostic examinations of superficial lymphatic abnormalities.