key: cord-0996724-t3tu1xkc authors: Uschnig, Christopher; Recker, Florian; Blaivas, Michael; Dong, Yi; Dietrich, Christoph F. title: Tele-ultrasound in the era of COVID-19: A practical guide date: 2022-01-10 journal: Ultrasound Med Biol DOI: 10.1016/j.ultrasmedbio.2022.01.001 sha: b462d72e19808df3c554ade79087de1bb1ca5e64 doc_id: 996724 cord_uid: t3tu1xkc Telemedicine has evolved over the past 50 years with video consultations and tele-health (TH) mobile apps now widely used to support care in the management of chronic conditions, but are infrequently utilized in acute conditions such as emergencies. In the wake of the COVID-19 pandemic, demand is growing for video consultations as they minimize health provider-patient interactions and thereby risk of infection. Advanced applications such as tele-ultrasound (TUS) have not yet gained a foothold despite having achieved technical maturity and availability of software offering from numerous companies for TUS for their respective portable ultrasound devices. However, ultrasound is indispensable for triage in emergencies and also offers distinct advantages in the diagnosis of COVID-19 pneumonia for certain patient populations such as pregnant women, children, and immobilized patients. Additionally, recent work suggests lung ultrasound can accurately risk stratify patients for likely infection when immediate PCR testing is not available and has prognostic utility for positive patients regarding need for admission and ICU treatment. Though currently underutilized, a wider implementation of TUS in TH applications and processes may be an important stepping-stone for telemedicine. The addition of ultrasound to TH may allow it to cross the barrier from being an application mainly used for primary care and chronic conditions to an indispensable tool used in emergency care, disaster situations, remote areas, and low-income countries where it is difficult to obtain high quality diagnostic imaging. The objective of this review is to provide an overview of the current state of telemedicine, insights into current and future use scenarios, its practical application as well as current TUS uses and their potential value with an overview of currently available portable and handheld ultrasound devices. In the wake of the COVID-19 pandemic we point out an unmet need and use case of TUS as a supportive tool for health care providers and organizations in the management of affected patients. patient interactions and thereby risk of infection. Advanced applications such as teleultrasound (TUS) have not yet gained a foothold despite having achieved technical maturity and availability of software offering from numerous companies for TUS for their respective portable ultrasound devices. However, ultrasound is indispensable for triage in emergencies and also offers distinct advantages in the diagnosis of COVID-19 pneumonia for certain patient populations such as pregnant women, children, and immobilized patients. Additionally, recent work suggests lung ultrasound can accurately risk stratify patients for likely infection when immediate PCR testing is not available and has prognostic utility for positive patients regarding need for admission and ICU treatment. Though currently underutilized, a wider implementation of TUS in TH applications and processes may be an important stepping-stone for telemedicine. The addition of ultrasound to TH may allow it to cross the barrier from being an application mainly used for primary care and chronic conditions to an indispensable tool used in emergency care, disaster situations, remote areas, and low-income countries where it is difficult to obtain high quality diagnostic imaging. The objective of this review is to provide an overview of the current state of telemedicine, insights into current and future use scenarios, its practical application as well as current TUS uses and their potential value with an overview of currently available portable and handheld ultrasound devices. In the wake of the COVID-19 pandemic we 3 point out an unmet need and use case of TUS as a supportive tool for health care providers and organizations in the management of affected patients. Key Words: telemedicine, handheld ultrasound device, lung ultrasound Telemedicine, a concept that originated in the late 1800s and early 1900s, is broadly understood as a means to exchange information for diagnosis, treatment and prevention of disease and injuries for patients, but also for research and evaluation as well as continuous education of health care providers (Strehle and Shabde 2006, Telematics 1998) . In contrast to traditional face-to-face or telephone consultations, telemedicine consultations also known as virtual consultations are increasing in demand. They allow the provision of remote medical care with specialized medical mobile apps or more recently video-chat capable apps including WhatsApp, Skype, or Face-time in certain countries (Armfield, et al. 2015 , Greenhalgh, et al. 2016 ). In 1957, a Canadian doctor constructed a teleradiology system in Montreal where radiographic images have been sent from one hospital to another five miles away through coaxial cable. In the early 2000s first remote ultrasound scans were done by astronauts with remote guidance from experts in the Mission Control Center (Sargsyan, et al. 2005) . Those ultrasound systems were capable of high-definition sonographic imaging for cardiac, vascular, general, abdominal, thoracic and musculoskeletal (10). Arbeille et al. developed and tested a Robotic arm to which an echographic probe was fixed, on a population of patient located in rural areas. The system was used on various adult pathologies (Gall bladder lithiasis, renal 4 cavity distension, appendicitis, superficial and deep vessels), as well as gynecology and fetal development (Arbeille, et al. 2007 . The technology remains relevant in aeronautics. The NASA continued to generate studies on the use of ultrasound by non-physician crew members at the International Space Station, which entailed prior training in ultrasound (Kwon, et al. 2007 , Law and Macbeth 2011 , Marsh-Feiley, et al. 2018 , Sargsyan, et al. 2005 . Currently, for routine ultrasound onboard the International space station a system with motorized probe sensors (titling rotating) controlled from the ground is in use that solely requires the astronaut to maintain a motorized probe motionless on himself for the duration of the examination (Arbeille, et al. 2018) . Before being sent to the space station the echo with motorized probe was successfully tested on 100 isolated patients on earth (Arbeille, et al. 2016 ). Often used complementarily with traditional face-to-face primary care, virtual consultations offer distinct advantages; they are considered to be more patient-centered and are perceived as being high quality by patients (McGrail, et al. 2017) . Additionally, the diagnostic accuracy of consultations is non-inferior to traditional in-person visits (Ohta, et al. 2017 , Sept, et al. 2020 though even shorter (Ignatowicz, et al. 2019) . Finally, virtual consultations are also popular with healthcare providers (Shaw, et al. 2018) . TH solutions are widely used in the management of chronic conditions such as diabetes, hypertension, asthma, and chronic obstructive pulmonary disease (Car, et al. 2020) . In obstetrics and gynecology, several successful pre-natal tele-ultrasound projects were completed (Chan, et al. 1999 , Ferlin, et al. 2012 ). Many regions have only a limited number of qualified fetal-medicine specialists who are capable of pre-natal ultrasound imaging. Thus, few physicians do not adequately cover demand for imaging that is critical for diagnosing and 5 preventing potential birth defects. Studies mainly from remote areas such as rural Australia have documented the need for fetal therapy and impact of TUS (Soong, et al. 2002) . Recently, a TUS system was also successfully tested in Peru that can be deployed to improve access to diagnostic imaging in low-resource areas (Marini, et al. 2021 ). However, in acute conditions such as in emergency or disaster situations telemedicine is used to a much lesser extent, although it can add value as part of triage protocols and management for patients who may benefit from immediate transportation. This includes triage of severe burn victims (Gacto-Sanchez, et al. 2020) , ocular emergencies (Car, et al. 2020) or stroke (Wilcock, et al. 2021) . Some reports suggest that the use of telemedicine improves diagnosis and management, but has less impact on mortality and complications in trauma patients (Lapointe, et al. 2020 ). However, a more recent large-scale representative study demonstrated that a telemedical consultation had significant impact on patients treated for stroke; resulting in a lower mortality rate with the largest benefit seen in smaller hospitals, among rural residents, and patients above the age of 85 (Wilcock, et al. 2021) . TH solutions may be utilized more in acute conditions if diagnostic imaging capabilities are expanded and embedded in telemedicine solutions. Here, we consider two scenarios offering distinct advantages by combining TH and advanced medical diagnostics, specifically ultrasound imaging. First, we examine use in trauma patients where ultrasound examinations are already standard procedure for triage. Second, we look at COVID-19 patients for assessing disease progression with lung ultrasound where computerized tomography (CT) or chest X-Rays are not an available or a viable option such as in remote areas, not medically indicated (such as in pregnancy), or unfeasible due to immobility or other causes. According to the World Health Organization (WHO), medical imaging is needed for making a diagnosis in 20 to 30% of clinical cases and ultrasound and/or conventional radiography are sufficient for 80 to 90% of those cases, yet two thirds of the world population have no access to medical imaging (Smith and Brebner 2002) . As telemedicine has evolved over the last few decades, medical imaging and therefore ultrasound technology have matured in parallel (Wootton 2001) . Ultrasound can be used at the patient's bedside and is more portable than other imaging technologies such as X-Ray, CT, or Magnetic Resonance (MR) imaging. TUS is defined as the use of ultrasound with voice and video and an additional instructor, such as an ultrasound certified physician, who is remotely connected to it (Chimiak, et al. 1995) . The utilization of TUS has been increasing globally over the last 20 years and various systems for remote ultrasound have been developed with the objective to provide ultrasound diagnosis to remote patient populations as well as in hostile environments. Ultrasound can be performed using the "remote guidance" method where an ultrasound expert guides and assists through voice commands a medical doctor or subject to orient the probe (Hamilton et al 2011). More recently echograph with probe orientation and echograph setting and function controlled from away Currently allow for quicker ultrasound investigation and images of higher quality (Arbeille, et al. 2018 , Arbeille, et al. 2016 . TUS is most used for emergency, abdominal and obstetrical ultrasound by general practitioners in remote areas where it has proven most successful. However, much of the available data focuses on emergency ultrasound (Su, et al. 2008 ) and other point-of-care ultrasound (POCUS) uses. TUS performed in resource-limited settings showed diagnostically satisfactory image quality that has an impact on medical treatment and outcome (Britton, et al. 7 2019). Use scenarios of TUS include rural pre-hospital settings, geographically remote areas, areas restricted due to political conflict, refugee camps, regions with limited medical professionals, or physicians not trained in ultrasound imaging (Adhikari, et al. 2014) . The technology itself matured over years, coincidentally with improved access to high bandwidth networks globally, thereby allowing high quality live-image transmission. Favorably for TUS, high bandwidth infrastructure is now often available even in many low-income countries. However readily available technology and regulatory challenges regarding data sharing and storage of patient data are still a major concern in many locations. Although TUS has distinct advantages and use-scenarios, we wanted to provide a comparison table of its strengths, weaknesses, opportunities and threats, created through an exploratory SWOT analysis with research into current literature, practical experience in TH, and testing a series of portable and handheld ultrasound devices (see Table 2A and 2B). Here, we narrowed our scope to more practical aspects such as portability of the ultrasound device, ease of use, acquisition and ongoing costs, availability, and technical advances. Generally considered as one of the biggest strengths of TUS, is the fact that no expert knowledge is required to start and operate an ultrasound device in order to generate an image that can be transmitted live and accurately interpreted by an ultrasound trained medical professional. Another limitation is reported that even experts who daily perform ultrasound examinations on-site may need twice as long for TUS compared to a conventional ultrasound. This is due to additional software needed to establish a remote connection, configurate the device remotely, instruct and guide the distant operator. This may put an additional burden on the health system from a financial perspective. Major advances in telecommunication technology have paved the way for TUS in mobile (Levine, et al. 2016 ) and web-based applications (Yoo, et al. 2004) . Commercially available video chat software can transmit high-quality and clinically useful ultrasound images, but may not guarantee compliance with local data safety and privacy rules. Studies show that images obtained are non-inferior to images captured with a stationary ultrasound device (Barreiros, et al. 2014 , Barreiros, et al. 2019 . Some mobile ultrasound applications go beyond solely projecting a live image but have built-in tools to grade images captured, allowing evaluation if the operator failed or passed in completing a proper image acquisition. Comparatively, more than two decades ago when bandwidth was limited to about 2Mbit/s, TUS could already be used successfully in obstetrics (Chan, et al. 1999 ). Ten years ago, transmission of real-time ultrasound video footage to a remote phone was shown to be feasible even with inexpensive equipment without sacrificing image quality on 3G networks (Liteplo, et al. 2010) . Today, availability and wide coverage of 4G networks are considered standard in many countries and certainly in developed countries, where 5G is currently being rolled out more widely. However, low bandwidth requirements are certainly an advantage, particularly in remote and isolated areas as well as in countries that lack the financial resources to expand and/or maintain high bandwidth networks. To further improve TUS images in sonographic evaluation, a quality assessment tool was developed to standardize quality of images obtained (Bahner, et al. 2011 ). An important feature 9 of the tool is to quantify the sonographer's influence in regard to the final image quality. This approach can also be adopted for TUS. In addition, more recently, software-based applications have been introduced that support the teaching of knobology and handling of the probe (Kirkpatrick, et al. 2016 ). In many cases, optimizing imaging quality requires fine adjustments of the probe such as a two or three-degree tilt or movement of the probe by just half a centimeter which can often be difficult to communicate verbally. With the aforementioned "remote guidance" method the remote operator is required to go through various steps to better ensure that. Another method requires the operator to manually perform a tilt movement with the probe (+/-45°) whereby all images of the organs below are captured and reconstruction in 3D at the expert center (Arbeille et al 2014) Moreover, Robotic systems have been developed that allow the examiner to remotely control the orientation of the probe with a robotic arm (Arbeille, et al. 2007 , Avgousti, et al. 2016 , Avgousti, et al. 2016 , Courreges, et al. 2005 . for reliable echographic and echocardiographic imaging (Arbeille, et al. 2014 , Georgescu, et al. 2016 . Lastly the echograph with probe orientation and echograph setting and function controlled from away allow real-time tele echography in a more comfortable manner as the motorized probe volume is similar to a 3D probe one thus much smaller than the robotic arm (Arbeille, et al. 2018 , Arbeille, et al. 2016 ). In a tele-guided setting, there are several ways to record and save images obtained and examination results. Various ultrasound documentation programs on portable devices and guidelines of how to appropriately document an ultrasound examination are available 10 (Dormagen, et al. 2015) . Moreover, cloud-based monitoring systems are able to circumvent the requirement for bedside supervision and documentation, which may expand the supervision capacity of physicians studying and documenting ultrasound images (Canty, et al. 2019 ). However, data security is a major concern regarding cloud-based documentation applications though recent cloud-based products comply with EU laws on data protection and privacy. A major threat for telemedicine in general is how patient data is stored and processed. As the value of personalized data increases and cheap data storage is abundantly available, telemedicine companies are able to record and analyze a whole set of parameters longitudinally in real-time whereby patients' access to and control over these stored data are not guaranteed. These developments should spark an intense public discourse, which seems to, at best, lag behind the staggering pace of technological advancement. A lack of health professionals trained in ultrasound imaging remains a substantial challenge to be addressed. This is particularly true for low-income countries, especially in rural areas and/or areas with a low population density, where ultrasound trained physicians are critically needed due to a general lack of other accessible advanced medical imaging diagnostics such as MR or CT imaging (LaGrone, et al. 2012, Parker and Harrison 2015) . Rapid technical development and competition in the field of medical software engineering have made costs manageable although prices vary significantly for devices and services offered (see Table 1 ) (Nascimento, et al. 2016 ). However, a cost-efficient alternative is readily available tools such as web interfaces or commercial messenger tools. They can be used for telesupported ultrasound with the additional advantage of being independent of any specialized 11 setting, and having the flexibility to perform ultrasound (Robertson, et al. 2017 ). However, consideration should be given to regulatory and data security concerns as indicated locally. Depending on the setting, different ultrasound devices offer various advantages, yet to our knowledge, there is no detailed overview available. Table 2 The provided overview of devices does not claim to be exhaustive -neither in regard to the devices under consideration nor in terms of applied criteria. As an indicator of "portability" weight, size, and number of probes needed for different ultrasound examinations were included; allowing for a more accurate estimation of the overall acquisition costs as well as total size and weight of the equipment. Other indicators "ease of use" and "versatility" are reflected in connectivity, available applications, and software supporting the device. Though image quality was not compared between devices, technical capabilities are listed within the technical features column, probe functionality, and tools. For a wide rollout of those devices, total acquisition costs and longevity of the device which includes free and long-term support of the software and mobile devices are crucial, but are beyond the scope of this review, and was not taken into account as there was no data. In the 1990s, ultrasound developed into a bedside application that was used in particular by emergency physicians for its ability to provide fast, accurate, and critical information during initial patient evaluation and working diagnosis (Jehle, et al. 1993) . For the detection and characterization of pleural fluid, POCUS is more sensitive than physical examination and chest X-rays. FAST ("Focused Assessment with Sonography for Trauma") has replaced peritoneal lavage as diagnostic tool of choice for abdominal trauma and is now considered standard practice (Song, et al. 2013) . A study showed that participants could perform a FAST scan in under six minutes and were able to obtain good quality images at the end of a 5-hour course. It was concluded that even a small number of tele-guided teaching sessions could significantly improve physician ultrasound skills in handling trauma patients. Since ultrasound is widely used in emergency medicine, POCUS examinations like FAST have been one of the first modalities that were successfully taught in TUS education (Song, et al. 2013) . Though promising in studies, TUS as a tool is underutilized in trauma medicine but may have a significant impact on mortality and the prevention of long term-disability. Moreover, studies demonstrated that even ultrasound-naïve medical professionals are able to obtain interpretable FAST TUS images within 5 minutes under remote guidance by an emergency physician that can be accurately assessed remotely (Boniface, et al. 2011 , Marsh-Feiley, et al. 2018 , Song, et al. 2013 . Even in a highly complex simulated disaster scenario with limited resources, commercially available mobile phones were adequate for physicians to accurately interpret FAST tele ultrasound images within 90 seconds of video transmission (Boniface, et al. 2011 ). TH solutions in general became significantly more widely available and utilized in health systems globally over the last year, used as an infection control method in the COVID-19 pandemic to minimize health provider-patient interactions to the most necessary procedures (Adans-Dester, et al. 2020) . In agreement with previous reports, we strongly suggest the promotion of lung TUS in order to reduce nosocomial outbreaks as it reduces exposure of health-care workers with patients and restricts patient movement (Buonsenso, et al. 2020 ). Caution must be exercised when using ultrasound to examine patients with pneumonia. Depending on the stage and progression of pneumonia trapped air could cause potential unknown damage and caution must be exercised as there is no comprehensive evidence-based study in this area. Hence, it's recommended to keep the Mechanical and Thermal Index levels as low as possible during the examination. Table 3 summarizes some advantages of lung ultrasound as it relates to COVID-19. Interstitial lung diseases are one of the most common consequences of COVID-19, and can cause acute respiratory distress syndrome (ARDS). In order to establish a diagnosis for those diseases to evaluate the course and progression of the disease, but also to guide treatment, imaging, usually in the form of a CT scan of the chest, i required (Bernheim, et al. 2020 ). The German professional societies for intensive care' recommend systematic bedside examinations with ultrasound for severe COVID-19 patients who are requiring intensive care. Currently, it is suggested that lung ultrasound examinations are performed systematically by scanning the lung, from medial to lateral or divide the thorax into left and right (hemi-thorax) and subdivide each side into four additional quadrants (Gargani and Volpicelli 2014 , Kluge, et al. 14 2020 , Soldati, et al. 2020 , Volpicelli, et al. 2012 . A standardized examination approach has been proposed by the ultrasound societies of Austria, Germany, and Switzerland. It is suggested that chest CT suspected lung changes due to COVID-19 should be confirmed and compared by lung and thoracic sonography of the suspected areas (Ai, et al. 2020 ). Though by no means a portable solution, currently chest CT-scans represent the gold standard to assess COVID-19 pneumonia and disease progression at this point (Kwee and Kwee 2020) . However, lung ultrasound is considered a highly valuable alternative in many settings and being portable offers a completely different set of opportunities for diagnosis and/or treatment. However, expert knowledge in assessing COVID-19 pneumonia is less widespread compared to chest X-ray or CT-scans for various reasons (Borakati, et al. 2020) . Previous studies confirmed the accuracy of lung ultrasound in detecting the occurrence and development of lung inflammation in bacterial and viral pneumonia as well as in acute respiratory distress syndrome. It was shown as being non-inferior to chest X-ray and to have value in disease follow-up (Dietrich, et al. 2015) . Particularly, POCUS was shown to be useful for the diagnosis of a SARS-CoV-2 infection (Gil-Rodrigo, et al. 2020 ). Lung-ultrasound already had a dedicated niche, one that may expand. In immobilized patients imaging already heavily relies on ultrasound in general as CT scans are not feasible due to the bulk and size of the device that is not portable. Similarly, in pregnant women and children CT scans are not routinely used due to high radiation exposure (Wu, et al. 2020) . In those cases, the only meaningful option for imaging COVID lung manifestation is ultrasound and further through TUS. A recent study showed that women infected with SARS-CoV-2 during 15 pregnancy were examined with lung ultrasound prior to giving birth and after with a CT for lung manifestations where a significant positive correlation between the two techniques was shown and lung ultrasound is considered as a safe alternative in pregnancy (Porpora, et al. 2021) . In children, the accuracy of lung-ultrasound in detecting pediatric pneumonia of any etiology seem to be comparable in the context of COVID-19 and is limited. Further studies are needed to assess usefulness of POCUS in children suffering from COVID-19 (Sainz, et al. 2021 ). Safe management procedures for the evaluation of suspected COVID-19 cases were suggested for lung ultrasound imaging at the bedside with standard personal protections per WHO indications. Those procedures can be similarly applied with health professionals executing lung TUS with a video consultation (Buonsenso, et al. 2020) . A more recent study showed that robot-assisted TUS over 5G is feasible and offers a significant advantage, as it protects also the examiner who is not necessarily a physician in TUS entirely from SARS-CoV-2 infection. However, such sophisticated devices are out of reach for the majority of health systems due to high acquisition costs, lack of portability, and high requirements on mobile networks to operate optimally (Wu, et al. 2020) . Given the advantages of TUS, we consider imaging of COVID-19 a highly valuable tool in diverse settings; particularly in under resourced health systems, restricted and/or remote areas such as refugee camps where portable ultrasound combined with a TH application may be the only viable option for an accurate assessment and/or confirmation of COVID-19 pneumonia and imaging at all, respectively. TH is a valuable and valued tool for patients and providers alike. It has matured technologically to a point where its current theoretical limitations are now centered mostly on legal, regulatory and data privacy concerns. The COVID-19 pandemic has stimulated all areas of healthcare to identify ways to limit the spread of infection, and TH was naturally adopted early on in the pandemic as tool for infection control that limit contact between patient and provider. As a result, TH saw a huge increase in demand and access to a wider medical audience and patients than ever before. Integrating TUS into TH, as a technologically sound tool in terms of diagnostic accuracy and image quality that is non-inferior to traditional ultrasound examinations, is a logical progression to enhance TH capabilities. Consequently, adding ultrasound to the list of TH services offered by practitioners, clinics, and mobile health companies might be a natural advancement of telemedicine. Regarding devices offering the greatest TUS value, multiple different aspects need to be considered and purchasing decisions will depend on clinical setting and actual intended use. In the case of COVID-19 lung TUS, we anticipate that remote areas or areas with limited access to a functioning healthcare infrastructure such as a refugee camp may greatly benefit from its use. In this particular use case, a handheld ultrasound device supporting multiple mobile operating systems with low acquisition costs, a long battery life, and included TH software for video consultations might be best equipped to deal with such a diverse patient population as one finds in refugee camps. Though studies have shown the benefits of TUS in general, large-scale studies are needed in the field to further explore weaknesses and strengths in different use-scenarios, obstacles with the equipment, and acceptance by patients and providers. For wider adoption of TUS private TH companies and clinics need to find a common standard that would allow different TUS devices to live stream and capture ultrasound images instead of proprietary software solutions from individual ultrasound device manufacturers. We have gotten protocol approval from our institutional review board. All the cited studies had IRB approval. Table 3 This table provides Can mHealth Technology Help Mitigate the Effects of the COVID-19 Pandemic? 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