key: cord-0784011-00j7okil authors: Marco, Allinovi; Alberto, Parise; Martina, Giacalone; Andrea, Amerio; Marco, Delsante; Anna, Odone; Andrea, Franci; Fabrizio, Gigliotti; Silvia, Amadasi; Davide, Delmonte; Niccolò, Parri; Angelo, Mangia title: Lung ultrasound may support diagnosis and monitoring of COVID-19 pneumonia date: 2020-07-20 journal: Ultrasound Med Biol DOI: 10.1016/j.ultrasmedbio.2020.07.018 sha: 6b447bbdefe5822cfb0aa6b09dd533f25bb93113 doc_id: 784011 cord_uid: 00j7okil The Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) disease (COVID-19) is characterized by a severe pneumonia and/or acute respiratory distress syndrome (ARDS) in about 20% of infected patients. Computed tomography (CT) is the routine imaging technique for diagnosis and monitoring of COVID-19 pneumonia. Chest CT has high sensitivity for diagnosis of COVID-19, but is not universally available, requires infected or unstable patient to be moved to the Radiology unit with potential exposure of several people, CT room needs proper sanification after use, and is underutilized in children and pregnant women for radioexposition concerns. The increasing frequency of confirmed COVID-19 cases is striking, and new sensitive diagnostic tools are needed to guide clinical practice. Lung ultrasound (LUS) is a non-invasive, bedside and emerging technique for the diagnosis of interstitial lung syndrome by evaluating and quantifying the number of B-lines, pleural irregularities and nodules or consolidations. In patients with COVID-19 pneumonia, LUS shows a typical pattern of diffuse interstitial lung syndrome, characterized by multiple or confluent bilateral B-lines with spared areas, thickening of the pleural line with pleural line irregularity, and peripheral consolidations. LUS showed to be a promising tool for the diagnosis of COVID-19 pneumonia, and LUS findings fairly correlate with chest CT scan. Compared to CT, LUS have several other advantages, such as preventing exposure to radiation, bedside repeatability during follow-up, low-cost and easier application in low-resource settings. Consequently, LUS may decrease utilization of conventional diagnostic imaging resources (CT scan and chest X-ray). LUS may help for early diagnosis, therapeutic decisions and follow-up monitoring of COVID-19 pneumonia, particularly in critical care setting, pregnant women, children and patients in areas with high rates of community transmission. SARS-CoV-2 disease is characterized by severe pneumonia and/or acute respiratory distress syndrome (ARDS) in about 20% of infected patients (Huang et al. 2020a , Chen et al. 2020a , with high morbidity and mortality. Herein, we provide an overview of the role of lung ultrasound (LUS) in the early diagnosis, therapeutic decision-making process and follow-up monitoring of COVID-19 pneumonia, representing a reliable alternative to computed tomography (CT) in this setting. Cited retrospective and prospective human studies had institutional review board (IRB) approval. Publications without IRB approval are in compliance with the Declaration of Helsinki. Chest CT is considered the routine imaging technique for diagnosis and monitoring of COVID-19 pneumonia. Patients with confirmed COVID-19 pneumonia have characteristic CT features: ground-glass or fine reticular opacities, reticulation, subpleural consolidations, vascular thickening, and/or traction bronchiectasis, with peripheral distribution, bilateral involvement, lower lung predominance, and multifocal distribution , Bai et al. 2020 ). Chest CT shows high specificity (Bai et al. 2020 ) and high sensitivity for diagnosis of COVID-19 pneumonia, being helpful in early screening of both symptomatic and asymptomatic highly suspected cases (Chen et al. 2020a , and in patients before negative-topositive conversion of the reverse-transcription polymerase chain reaction (RT-PCR) (Ai et al. 2020 . However, in different studies, 20/36 (56%) positive adult patients in the first 2 days after clinical onset , 8/99 (8%) symptomatic adult patients with history of exposure to confirmed cases ) and 12/24 (50%) asymptomatic positive carriers had no abnormal CT findings. Moreover, CT scan is not universally available in Emergency departments and is a suboptimal option in paediatric setting because of the exposure to high-dose radiation and the frequent need of sedation (Miglioretti et al. 2013) . Furthermore, in a recent systematic review including 4612 children with COVID-19, 85.7% underwent chest CT scan, and 36% of them had no pathological CT findings (Liguoro et al. 2020) . The increasing frequency of confirmed COVID-19 cases is striking, and new highly sensitive diagnostic tools are needed in clinical practice. This is particularly true considering that most of the affected/contagious patients are asymptomatic or experience mild symptoms ), RT-PCR has a sensitivity of only 71% for SARS-CoV-2 infection (Fang et al. 2020 ) and a considerable proportion of patients with COVID-19 pneumonia shows normal chest radiographs at onset (Yoon et al. 2020 , Ng et al. 2020 . Several data have shown that LUS is a non-invasive, bedside and emerging technique in the diagnosis of interstitial lung syndrome by evaluating and quantifying the number of B-lines, pleural irregularities and nodules or consolidations (Soldati and Demi 2017 , Volpicelli et al. 2012 , Demi et al. 2020a . LUS show numerous artifacts which physicians recognize and evaluate as part of their diagnosis (Demi et al. 2020b ): A-lines are motionless and regularly spaced horizontal lines to the pleura (Fig.1a) , and correspond to normal reverberation artifacts of the pleural line; B-lines are vertical linear artifacts that arise from pleural line (Fig.1a) , likely representing ultrasound reverberations generated by the thickened interlobular septa and other subpleural structures (Volpicelli et al. 2012) . There are several different B-line shapes, e.g. single cone-shaped line (Fig.1b) , single thin line (Fig.1c) , or single thick line (Fig.1d) . Multiple B-lines are considered the sonographic sign of lung interstitial syndrome, and their number increases along with decreasing air content and increasing lung density. An inhomogeneous bilateral pattern of multiple coalescent B-lines and white lung, sometimes with scattered spared areas, characterizes ARDS (Soldati and Demi 2017) . Lung peripheral consolidations are subpleural echo-poor regions or with tissue-like echotexture (Fig.1e) , with different features: with or without air or fluid bronchogram, vertical artifacts at the far-field margin, or hepatization (Volpicelli et al. 2012) . Consolidations associated to B-lines are characteristic ultrasound patterns observed in patients with ARDS. In clinical practice, especially in critical care setting, several scoring systems have been proposed to quantify the extent of lung involvement, based on the number of chest wall zones of each system: 4-zone, 6-zone, 8-zone, 12-zone or 14-zone methods (figure 2) are mainly adopted in critical care setting. Using the 4-zone, 6-zone, or 8-zone scoring systems (Platz et al. 2019) , B-lines are counted in multiple intercostal spaces across the thorax, and 3 or more B-lines in a single intercostal space is defined "B-pattern". Differently, using the 12-zone scoring system, in each zone a score of 0 is assigned for no B-lines and a score of 1 is assigned for multiple spaced/isolated Blines, a score of 2 is assigned for diffused coalescent B-lines or "light beam", and a score of 3 is assigned for lung consolidation (Volpicelli et al. 2020) . Finally, using the 14-zone scoring system, in each zone a score of 0 is assigned for regular pleural line and A-lines, a score of 1 is assigned for a indented pleural line with vertical areas of white below each indent, a score of 2 is assigned for a broken pleural line with vertical areas of white below each small-to-large consolidated area, and a score of 3 is assigned for dense and largely extended white lung with or without larger consolidations (Soldati et al. 2020b ). Recently, an Italian consensus proposed a standardization for the international use of LUS for the management of patients with COVID-19 in order to use a well-validated terminology related to image artifacts and adopt objective clinical standards for interpretation of imaging features (Soldati et al. 2020b ). LUS scanning frequencies, technical adjustments, acquisition protocols, choice of different probes, and mechanical indexes have strong effects on the visualization and counting of lung Blines (Soldati et al. 2020b) , consequently LUS should be used by appropriately trained users only, in order to avoid misdiagnosis. LUS was shown to be a promising tool for the diagnosis and follow-up of pneumonia in adults as well as in children Copetti 2014, Pereda et al. 2015) . In a meta-analysis, LUS showed high accuracy in diagnosing pneumonia compared with chest CT scan (Long et al. 2017) . Moreover, LUS is now considered to have similar diagnostic performance for interstitial lung syndrome (interstitial pneumonia, interstitial diseases and ARDS) as chest CT (Man et al. 2019 , Patel et al. 2018 , Mayo et al. 2019 , Asano et al. 2018 , which is the gold standard method for the diagnosis. In particular, a comparative study by Lichtenstein et al. (2004) showed that the accuracy of LUS in patients with ARDS was 93% for pleural effusion, 97% for consolidation, and 95% for alveolar interstitial syndrome. However, the specificity of B-line evaluation at LUS is low, because B-lines can be visualized in any disease process causing interstitial lung disease (for example, mild to moderate lung congestion, pulmonary edema, pneumonitis, viral pneumonia, pulmonary fibrosis, ARDS) (Dietrich et al. 2016 , Demi et al. 2020a , Soldati et al, 2019 . Similarly, subpleural consolidations and pleural effusion, which represent anatomic alterations and not artifacts, show a low specificity for COVID-19 as they appear in many different conditions. Although the most frequent cause of interstitial pneumonia time in areas with high COVID-19 prevalence is the SARS-CoV-2, other causes remain possible (atypical bacteria, flu viruses, etc). In patients with COVID-19 pneumonia, LUS shows a typical bilateral pattern of diffuse interstitial lung syndrome, characterized by multiple or confluent B-lines with spared areas, thickening of the pleural line with pleural line irregularity (figure 3), and less frequently subpleural consolidations and pleural effusion (Soldati et al. 2020a , Poggiali et al. 2020a , Peng et al. 2020 , Huang et al. 2020b , Buonsenso et al 2020b , Volpicelli et al. 2020 , Volpicelli and Gargani 2020 , Lomoro et al. 2020 , Xing et al. 2020 , Nouvenne et al. 2020 , Yasukawa and Minami 2020 . In COVID-19 pneumonia, different degrees of interstitial syndrome and alveolar consolidation detected by LUS are directly correlated with the severity of the lung injury (Peng et. 2020 , Xing et al. 2020 ). There are currently no known pathognomonic findings of COVID-19 on LUS, although Volpicelli et al. recently reported the "light beam", a broad, lucent, band-shaped, vertical artefact which moves rapidly with sliding, corresponding to the early appearance of "ground glass" (Volpicelli et al. 2020, Volpicelli and Gargani 2020) . LUS can detect the pulmonary dynamic changes associated with COVID-19 pneumonia (Soldati et al. 2020a ). In the early stages, the main ultrasound finding is focal B-lines while, as the disease progresses, B-lines become multifocal and confluent (interstitial lung syndrome), with further development of clear consolidations (Soldati et al. 2020b , Fiala 2020 . During convalescence, B-lines and consolidations gradually disappear and are replaced by A-lines (Peng et. 2020 , Xing et al. 2020 , Denina et al. 2020 . In this setting, the findings on LUS appear to correlate well with the findings on chest CT scan in patients with COVID-19 pneumonia (Poggiali et al. 2020a , Peng et al. 2020 , Lu et al. 2020 , Huang et al. 2020b , Yang et al. 2020b , and can be expected to develop over a similar timeline (Fiala 2020) . The sensitivity, specificity and diagnostic accuracy of LUS showed to increase with the severity of COVID-19 pneumonia when compared to chest CT scan (Lu et al. 2020) . LUS allows for the evaluation of pleural and peripheral pulmonary lesions, while cannot detect lesions that are deep within the lung, as aerated lung blocks transmission of ultrasonography. However, studies on chest CT in patients with COVID-19 demonstrated that most of the consolidations are generally localized in the peripheral lung (Yang et al. 2020a , Yang et al. 2020b , which facilitates detection by LUS. Of note, in a comparative study with chest CT scan, LUS showed a lower specificity in differentiating patients with COVID-19 and non-COVID-19 pneumonia (Chen et al. 2020b) , considering that different pathogens can share similar LUS patterns. However, through rational integration of LUS with the clinical data, a good specificity can be achieved in case of LUS findings suggestive of COVID-19, in relatively young patients or in those without a history of lung disease, in the not-very-early stages of COVID-19 pneumonia (Soldati et al. 2020c ). Compared to CT, LUS has several advantages: it enables a bedside assessment, reduces the length of patient stay at the Emergency room (reducing healthcare workers exposure to infected patients), prevents exposure to radiation (especially for children and pregnant women), can be repeated during follow-up with low-costs and easy application in low-resource settings (Soldati and Demi 2017 , Volpicelli et al. 2012 , Denina et al. 2020 , Buonsenso et al. 2020a , Moro et al. 2020 ). Moreover, CT scan requires the patient, potentially infected and unstable, to be moved to the Radiology unit with potential exposure of several people, and proper sanification of CT room after use. The use of bedside LUS allows to integrate the information about the state of the lung (sonographic patterns) with all the information given from medical history and risk of exposure, clinical examination and blood exams, giving the physician a better characterization of the disease and helping decision-making process (Volpicelli et al. 2020 ). This multiparametric approach may increase the diagnostic accuracy of LUS for COVID-19 pneumonia, especially in mild to moderate disease or in differential diagnosis with non-COVID-19 pneumonia where LUS seems to have lower specificity compared to CT scan (Lu et al. 2020 , Chen et al. 2020b ). Although conclusive data on COVID-19 patients are still lacking, data from studies in different settings of interstitial pneumonia and ARDS may support the role of LUS, especially in areas with high rates of community transmission, guiding therapeutic decisions and procedures in patients with COVID-19 in many critical settings (Soldati et al. 2020b ): general practitioners, nursing homes, Emergency Department, General Internal Medicine Ward, Pulmonology Ward, Hemodialysis, pregnant women and paediatrics. Those general practitioners who are confident with LUS may represent a first important step in patients with clinical suspect of COVID-19 infection, in order to reduce unnecessary Emergency department visits. LUS might be a useful tool, providing an additional datapoint to the full clinical picture, especially if compared to the limited traditional chest auscultation (Copetti et al. 2016) , and allowing an advanced triage for COVID-19 directly at home (Shokoohi et al. 2020 , Soldati et al. 2020c ). The probe can be used as a stethoscope to scan any portion of the lung providing an increased diagnostic accuracy. Nursing homes are on the front lines of this pandemic, and their residents were decimated in several countries worldwide. LUS, with a portable ultrasound device, has proven to be an excellent tool for identifying COVID-19 in nursing home residents (Nouvenne et al. 2020) , suggesting a potential role for screening patients at high risk in a setting characterized by scarce diagnostic resources. In Emergency Departments or in COVID-restricted triage areas for patients with clinical suspect of COVID-19 infection, LUS used as a primary survey tool in the acutely dyspnoeic or hypoxemic patients provides an immediate evaluation of the lung (Zanobetti et al. 2020 , Volpicelli et al. 2020 . During COVID-19 pandemic, LUS, as part of a structured triage system in an emergency department, can help to early detect pulmonary and pleural findings even in patients without respiratory symptoms and/or fever, especially if pulse oxygen levels are lower than normal values (Poggiali et al. 2020b) . For a patient with respiratory failure, a normal LUS could rule out COVID-19 pneumonia and orientate to different diagnosis (Volpicelli et al. 2020) . Conversely, we suggest that patients with LUS findings suggestive for COVID-19 but negative RT-PCR results should be isolated, and RT-PCR should be repeated to avoid misdiagnosis (Soldati et al. 2020c ). In General Internal Medicine wards and Pulmonology wards, LUS might be useful for monitoring the effect of therapeutic drugs (immunosuppressive strategies, antiviral drugs or others) as a bedside and real-time technique, and may decrease utilization of conventional diagnostic imaging resources, reducing exposure of healthcare workers to SARS-CoV-2 (Yasukawa and Minami 2020). Patients on hemodialysis show increased risk of contagion and serious complications during COVID-19 pandemic (Alberici et al. 2020) , due to frequent contact with healthcare facilities and high comorbidity burden. Although patients on dialysis have multiple potential etiologies for dyspnea and multiple B-lines at LUS (such as heart failure and fluid overload) and for fever (such as vascular access infection), different LUS patterns detected in COVID-19 patients may help in differential diagnosis in this setting (Reisinger et al. 2020 , Vieira et al. 2020 ). In pregnant woman, LUS may represent a valuable tool alternative to CT scan during COVID-19 pandemic (Buonsenso et al. 2020a , Moro et al. 2020 , Youssef et al. 2020 , particularly if considering that is mandatory to avoid exposure to radiation in this specific setting, and that obstetricians and gynecologists are usually familiar with the use of ultrasound. In the paediatric setting, where LUS is considered as an imaging alternative to CT scan for the diagnosis of childhood pneumonia (Pereda et al. 2015) , LUS could play a central role in COVID-19 pandemic. In fact, LUS showed to be able to detect lung pathology in children (Denina et al. 2020 , Musolino et al. 2020 ) and neonates (Feng et al. 2020) with confirmed COVID-19, even when asymptomatic, with the same LUS patterns described in adults. Moreover, LUS showed to decrease utilization of conventional diagnostic imaging resources in children with suspected COVID-19 (De Rose et al. 2020) . The large number of asymptomatic and mild cases of COVID-19 in children (Parri et al. 2020; Lu et al. 2020) confirms that chest CT scan and X-ray should not be routinely used. However, further studies in children are needed because LUS showed conflicting results in early stages and mild forms of COVID-19 pneumonia (Musolino et al. 2020 , Scheier et al. 2020 ). Although the sensitivity and specificity of LUS in diagnosing COVID-19 pneumonia remains to be determined in larger studies, LUS represents a reliable alternative of CT scan and chest X-ray in all these settings. Efficient triage of patients with suspected COVID-19 at all health facility levels can help the national response planning and case management system cope with patient influx. In hemodynamically or respiratory unstable Intensive Care patients, LUS may have major utility for bedside management of COVID-19 in order to track the evolution of interstitial pneumonia and ARDS, to monitor lung recruitment maneuvers and response to therapies, to early identify possible complications (pneumothorax, over-infections), to guide several invasive procedures, and for making decisions related to weaning the patient from ventilator support (Peng et al. 2020 , Mojoli et al. 2020 . Although data in Intensive Care patients with COVID-19 are scarce, a practical approach based on LUS can be proposed to guide therapeutic decisions in ARDS patients (Bouhemad et al. 2015) and different LUS scoring systems may be used to estimate the extent of lung involvement (Volpicelli et al. 2020a) . In fact, an important reduction or absence of lung sliding and the evolution to consolidations indicate severe pneumonia or ARDS, suggesting that patient may require invasive ventilatory support Copetti 2014, Copetti et al 2008) . Moreover, LUS score, as an estimate of lung aeration, can be regularly monitored at the beginning and any time point after therapy for COVID-19 is started (i.e. positive end-expiratory pressure [PEEP] trial or prone position) (Conway et al. 2020 ). An increase in score and/or the presence of posterolateral/inferior consolidations indicate a decrease in aeration, suggesting the need for additional PEEP and recruitment maneuvers, while a decrease in score indicates reaeration, suggesting the success of interventions and eventually the decision to wean respiratory support (Conway et al. 2020) . To confirm this, although data on COVID-19 patients are still lacking, a PEEP-induced lung recruitment (Lichtenstein et al. 2004 , Bouhemad et al. 2011 ) and the response to prone positioning (Prat et al. 2016 , Wang et al. 2016 can be adequately estimated with bedside LUS in patients with ARDS. LUS can represent an useful tool to confirm endotracheal tube placement (Karacabey S et al. 2016 , Das SK et al. 2015 , particularly tricky in a COVID-19 area setting and when the End-tidal CO 2 device is not available, and to detect pneumothorax (Alrajab S et al. 2013) , that is frequently identified with an anterior extension in the critically ill patient in recumbent or semi-recumbent position. Even if pleural effusions are not frequent in COVID-19 patients, a bedside thoracentesis can be safely performed with an echo-guided technique, in order to promote lung recruitment and ameliorate oxygenation, and to reduce the incidence of peri-procedural complications (Rodriguez-Lima DR et al. 2020 , Mercaldi CJ et al. 2013 . LUS seems to be a safer and more convenient alternative to CT scans in a transportation limited setting like mechanical ventilation or even extracorporeal membrane oxygenation (ECMO). In an urgent situation like patients' situation deteriorates, a quick imaging tool is badly needed. In this setting, systematic application of LUS showed to decrease utilization of conventional diagnostic imaging resources (Pontet et al. 2019 , Vetrugno et al. 2020 , Mojoli et al. 2020 , Mongodi et al. 2020 . Personal protective equipment should be worn when it is necessary to scan a patient with suspected or confirmed COVID-19 infection. In order to minimise the risk of potential SARS-CoV-2 transmission, sonographers (1) should assume that every patient has COVID-19 infection; (2) should wear personal protective equipment, such as face masks (N95/FFP2 or FFP3), waterproof protective gear or goggle, disposable gown, one or two pairs of disposable gloves; (WHO 2020), (3) should drape the ultrasound machine with a plastic disposable wrap, also covering probes, cables, couch, and keyboard with disposable covers; (4) should clean and disinfect the equipment and room with alcohol-based disinfectant cleaner at the end of every exam. Compared to a portable X-ray or CT machine, ultrasound machines are faster to decontaminate due to their small size. Some physicians have reduced the risk of COVID-19 transmission and minimised decontamination time by using portable, hand-held wireless ultrasound probes attached to sheathed tablet devices, placed in two separate single-use plastic covers (Buonsenso et al. 2020b ). In the contest of COVID-19 pandemic, a portable ultrasound may represent a valuable tool considering that may be transported to remote areas, and can be easily sterilized. However, LUS should be used by appropriately trained users only, in order to avoid misdiagnosis, and prevent SARS-CoV-2 transmission due to non-adherence to appropriate cleaning and disinfection principles. LUS may be a first-line diagnostic imaging alternative to chest CT scan and chest X-ray during every step of COVID-19 disease, even before clinical manifestations, particularly in children, pregnant women, critically ill patients that cannot be moved, and patients in areas with high rates of community transmission. The combination of sonographic patterns at LUS with clinical and laboratory findings, followed by chest CT for confirmation in selected cases, may help for early diagnosis, therapeutic decisions and follow-up monitoring of COVID-19 pneumonia both in children and adults. Dr. Allinovi, Dr. Parise, Dr. Giacalone, Prof. Amerio, Dr. Delsante, Prof. Odone, Dr. Gigliotti, Dr. Franci, Dr. Amadasi, Prof. Delmonte, Dr. Parri, and Dr. Mangia report no conflicts of interest. This research received no specific grant from any funding agency in the public, commercial or notfor-profit sectors. Figure 1 . A-lines: horizontal lines to the pleura (Fig.1a) ; B-lines: linear vertical artifacts that arise from pleural line ( Fig.1a) with different B-line shapes, e.g. a single cone-shaped line (Fig.1b) , a single thin line (Fig.1c) , a single thick line (Fig.1d) , a subpleural consolidation without air bronchogram (Fig.1e) . 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