key: cord-280241-h16s6wwm
authors: McStay, R.; Johnstone, A.; Hare, S. S.; Rodrigues, J.C.L.; Nair, A.; Jacob, J.; Edey, A.; Robinson, G.
title: COVID-19: looking beyond the peak. Challenges and tips for radiologists in follow-up of a novel patient cohort
date: 2020-10-08
journal: Clin Radiol
DOI: 10.1016/j.crad.2020.09.025
sha: 
doc_id: 280241
cord_uid: h16s6wwm

As the coronavirus pandemic evolves, the focus of radiology departments has begun to change. The acute phase of imaging a new disease entity whilst rationalising radiology services in the face of lockdown has passed. Radiologists are now becoming familiar with the complications of COVID-19, particularly the lung parenchymal and pulmonary vascular sequelae and are considering the impact follow-up imaging may have on departments already struggling with a backlog of suspended imaging in the face of reduced capacity. This review from the British Society of Thoracic Imaging explores both the thoracic and extra-thoracic complications of COVID-19, recognising the importance of a holistic approach to patient follow-up. The British Thoracic Society guidelines for respiratory follow-up of COVID-19 will be discussed, together with newly developed reporting templates, which aim to provide consistency for clinicians as well as an opportunity for longer-term data collection.

The arrival of a global pandemic is a rare event in medicine. Yet the rate at which knowledge of coronavirus disease 2019 (COVID-19) has disseminated across today's globally connected world and the level of universal collaboration witnessed between medical specialties has been astonishing. As radiologists, we have rapidly rationalised services, designed new imaging pathways, and reorganised working J o u r n a l P r e -p r o o f patterns, whilst maintaining the "bread and butter" of urgent diagnostic work for patients, including those with COVID-19. Common imaging appearances of a new disease entity have been described, disseminated, and reported in a rapid and structured way, aiding the diagnostic and follow-up patient pathway.

In the UK, the peak of infection in early April has passed, with the number of new cases falling each day. As the country emerges from lockdown, radiologists now need to look forward and be ready for new challenges. Many departments benefitted from the brief interlude in scanning as breathing space to clear the existing backlog of reporting generated by a chronic shortage and underinvestment in the radiology workforce. Yet following this brief period of altered workflow, new challenges are emerging. Firstly, the imbalance between a new backlog of demand for previously suspended imaging and further reduced capacity due to increased scan time;

secondly, the recognition of a new patient cohort with post-COVID-19 complications who require a holistic approach to follow-up. It is this particular challenge associated with post-COVID-19 follow-up that will be the main focus of this article.

Following on from initial statements in the acute phase of the pandemic (1) (2), this update from the British Society of Thoracic Imaging group aims to provide an overview of the multisystem complications of COVID-19 with a focus on the thoracic manifestations, in particular the lung parenchymal and pulmonary vascular sequelae.

The authors will also explore the British Thoracic Society (BTS) guidance on the respiratory follow-up of patients with COVID-19, including the resource implications for departments, discuss the potential use of structured reporting of follow-up imaging and outline future opportunities for longitudinal data collection and research. The precise prevalence of post-COVID-19 complications in the UK is unknown and will be difficult to ascertain due to the lack of testing in asymptomatic and mildly symptomatic patients not admitted to hospital. Until there is widespread access to immunoglobulin testing with confirmation of the duration of maintenance of seropositivity, it will be impossible to know the denominator for this calculation. The only similarly investigated comparator groups are those with severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS). Data from these pandemics will provide a contextual background, particularly for the long-term pulmonary sequelae of COVID-19 (3) (4).

There is emerging evidence that patients with COVID-19 experience a higher rate of thromboembolic disease, both venous and arterial, with pulmonary embolism (PE) tending to be the most frequent thrombotic complication (5) (6). The inflammatory nature of this infection, together with hypoxia, immobilisation, and disseminated intravascular coagulation are all likely to contribute to this phenomenon (5) . Rare cases of arterial thrombus and cerebral vein thrombus have also been reported in association with COVID-19 infection (5) (Fig. 1) .

Respiratory failure in COVID-19 is poorly understood, with disparity between the severity of hypoxaemia and the degree of impairment in respiratory mechanics.

Although it would seem that acute respiratory distress syndrome (ARDS) is not J o u r n a l P r e -p r o o f responsible for all cases of respiratory compromise associated with COVID-19, it is one of the commonest reasons for transferring patients to critical care and is a major cause of death (7) . Its reported prevalence in COVID-19 is up to 31% (8) (9), significantly higher than rates of injury to other organ systems (Fig. 2) .

Respiratory infection in COVID-19 can be complicated by viral co-infection and secondary bacterial pneumonia, including ventilator-associated pneumonia.

Secondary bacterial pneumonia has been well studied in pandemic and seasonal influenza, when it contributes significantly to mortality (10) . In COVID-19, it can occur in the acute phase of the disease and also in the recovery period (11) . It is also more common in older patients, and in a retrospective study in China, it was reported in 15% of all patients and 50% of non-survivors (12) . Radiologists should be familiar with the classical and genuinely indeterminate features of COVID-19 on chest radiography (CXR) and computed tomography (CT) already described (2) and be alert to "non-COVID-19" findings such as lobar consolidation with air-bronchograms, more typical for bacterial pneumonia (Fig. 3) , and bronchial wall thickening, mucous plugging, and tree-in-bud changes, more typical of airway-centred infection (Fig. 4) .

Pneumothorax and spontaneous pneumomediastinum in COVID-19 are predominantly seen as case reports in the literature and are uncommon complications (13) . Pneumothorax was reported as a rare presenting sign (1%) in a case series of 99 patients in China (14) and has been recognised as a rare occurrence in progressive disease (7) (Fig. 5) . It is already established that pneumothorax and tension pneumothorax are recognised complications of J o u r n a l P r e -p r o o f mechanical ventilation, with a predisposition in patients with underlying lung disease and this would seem to hold true in COVID-19 pneumonia also (13) (15) . Spontaneous pneumomediastinum has been described in the literature and observed by the authors, and although it is rare in viral pneumonia, it was also reported in cases with SARS (16) (17) (Fig. 6 ).

Reports in the literature highlight both a high incidence of macrovascular injury (e.g., acute PE), but also microvascular injury in COVID-19. In a study by Klok et al. (5) , the incidence of thrombotic complications in 184 intensive care unit (ICU) patients with COVID-19 was 31%. Anecdotal reports from large UK critical care units suggest potentially higher figures. Autopsy findings from the first 12 consecutive COVID-19 deaths at a single German academic medical centre (18) revealed deep venous thrombosis in 58% in whom venous thromboembolism was not suspected, with PE a direct cause of death in four patients; however, COVID-19 has also been associated with microvascular coagulopathy, with findings similar to those seen in disseminated intravascular coagulopathy (19) . It would seem reasonable, therefore, to suggest that although patients may develop acute PE secondary to a severe illness and hospitalisation, the pronounced inflammatory response seen in a cohort of COVID-19 patients results in a substantial pro-thrombotic tendency.

There is insufficient literature on the use of dual-energy CT (DECT) in COVID-19 to know whether this technique provides additional assessment of microvascular disease in the form of "perfusion abnormalities" on iodine maps; however, Lang et al. (20) . This has also been the experience of some of the authors, who also note that when present, acute PE has often developed in segmental/subsegmental vessels, rather than in main or lobar pulmonary arteries.

It is possible (but still unknown) that those recovering from COVID-19 may develop chronic thromboembolic disease (CTED), chronic thromboembolic pulmonary hypertension (CTEPH) and/or pulmonary hypertension (PH) secondary to lung disease (e.g., fibrotic organising pneumonia).

It is important that both clinicians and radiologists be alert to the diagnosis of PH.

CTEPH particularly is under-diagnosed; in 2015 it was estimated that, on average, only 16% of patients in the USA, Europe and Japan who had CTEPH were diagnosed (21) .

Diameter of the main pulmonary artery (mPA) exceeding 30-31mm should raise the suspicion of PH; however, in the setting of established pulmonary fibrosis, a ratio of the mPA to the adjacent ascending aorta >1.1 may be a more reliable predictor (22) (23) (24) . The presence of increased pulmonary artery to bronchus ratio in at least three vessels has also been shown to have a high specificity for the diagnosis of PH (25) . A right ventricle to left ventricle ratio (RV:LV) >1.0 has consistently been shown to be a useful risk stratification biomarker and predictor of poor outcome in acute PE, CTEPH, and interstitial lung disease (25) (26) (27) (28); however, the RV:LV ratio is substantially under-reported, as highlighted in the 2019 National Confidential Enquiry into Patient Outcome and Death (NCEPOD) (29) . These findings, together with reflux of contrast medium into the hepatic veins, may be present in all forms of PH, irrespective of aetiology. In CTED/CTEPH, the radiologist should review the J o u r n a l P r e -p r o o f pulmonary arteries for vascular webs and occlusions (Fig. 7) . DECT may also show multiple peripheral perfusion defects (Fig. 8) . The lung parenchyma can often show mosaic attenuation with geographic areas of low attenuation associated with peripheral scarring, the residuum of previous infarction (Fig. 9 ). Subtle pulmonary vascular abnormalities, particularly those observed in more distal chronic thromboembolic disease can be difficult to detect with CT and, as in the work-up of suspected PH, ventilation/perfusion scintigraphy (VQ) should be considered a more sensitive imaging tool to exclude chronic thromboembolic disease, if this is suspected (30) .

CXR follow-up will suffice for the majority of COVID-19 patients, and should show improvement or even total resolution of abnormalities detected in the acute phase. In the absence of robust analyses to date, it is reasonable to expect that COVID-19 follows a similar pattern of recovery and debilitation to SARS, where follow-up (after a mean of 6.5 weeks) suggested approximately 20% of patients could have residual CXR and HRCT abnormalities, usually accompanying a physiological deficit.

It is worth remembering that, if guidance is dutifully followed, patients undergoing CT follow-up should be those who had a protracted or critical course of illness and have insufficiently improved, suggesting that a high pre-test probability of abnormality on CT could be expected. The key aims of parenchymal CT evaluation post-COVID-19 are (1) to identify any realistic chance of stabilising or even reversing active inflammation in the lung; and (2) to detect residual fibrosis, both of which should prompt consultation with interstitial lung disease (ILD) teams, to consider whether immunomodulatory or even anti-fibrotic therapy could be appropriate.

CT follow-up experience thus far mirrors that of preliminary reports (31) .

Unsurprisingly, patterns of fibrosis or diminishing abnormality with no fibrosis representing the organising/fibrotic and resolving phases of lung injury, respectively, are seen to different extents and often co-exist in the same patient. The cardinal signs of fibrosis (traction bronchial dilatation with architectural distortion and volume loss) can be noted, together with reticulation, and may be either bronchocentric or peripheral, usually reflecting the distribution of the acute abnormality. A perilobular pattern of organising pneumonia (32) , recognised in the acute phase of the disease, may also be present on follow-up but may dissipate on later imaging, especially if unaccompanied by signs of fibrosis (Fig. 10) . It is worth noting that if CT is performed too early following the acute phase of the infection, transient architectural distortion and even apparent traction dilatation within areas of radiological organising pneumonia may be spuriously present, leading one to overcall fibrosis, but this can subsequently return to normal. Conversely, ground-glass opacity (GGO) with no signs of fibrosis (so-called "free-standing GGO") may be seen and reflect a lingering inflammatory infiltrate, or perhaps even a superimposed viral infection, as it may do in ILD (33) (34) . Radiological distinction of these two underlying causes of GGO is virtually impossible and relies on correlation with the patient's clinical course and other laboratory parameters; however, the presence of such freestanding GGO could prompt physicians to consider additional investigations, including bronchoalveolar lavage to aid therapeutic decision-making, particularly as consideration of immunomodulatory therapy requires careful negotiation of a precarious risk-benefit balance after recent infection or in the presence of an opportunistic infection. As such, it seems sensible to provide a pragmatic estimate of whether the pattern on CT J o u r n a l P r e -p r o o f is predominantly fibrotic or inflammatory, and to use all available tools, for example sagittal reformats, (Fig. 11) to assess for early signs of volume loss.

COVID-19 is predominantly a respiratory disease mostly affecting adults. In most people who experience symptoms, the illness is mild but it may progress to pneumonia, ARDS, multi-organ failure, and death (35) ; however, over the course of 3 months, we have begun to disentangle the wider multisystem effects of this disease.

These have included coagulopathy (as described above) (18) , and damage to the cardiovascular (36) (37), neurological (38) , and renal systems, making a multidisciplinary evaluation, including mental health and rehabilitation, key aspects of patient management. The extent to which radiology input will be required for the diagnosis and follow-up of extra-thoracic COVID-19 complications is uncertain.

Cardiac complications including left ventricular dysfunction, arrhythmias, and myocardial injury are common in patients with pneumonia and have also been seen with COVID-19 (39) . Studies report acute myocardial injury in 12-17%, inferred from an elevation of cardiac biomarkers (12) (40) (41) and there are also case reports and case series of myocarditis (42) (43) (Fig. 12 ). Myocardial damage originating from COVID-19 can relate to the cytokine storm initiated by the body's immune response to the virus, or from virus-mediated damage to the heart itself (44) . Cardiac involvement has recently been described in recovered COVID-19 patients, with cardiac MRI showing myocardial oedema, fibrosis, and impaired right ventricular function (45) . Furthermore, COVID-19 is now known to affect children (46) and rare case reports of Kawasaki's disease in patients who also tested positive for SARS J o u r n a l P r e -p r o o f CoV-2 have been published (47) , although there is no evidence of a definite causal association (48) .

Acute kidney injury is frequently observed in COVID-19 and is an independent predictor of mortality (49) .

Gastrointestinal (GI) symptoms are also recognised, sometimes in the absence of respiratory manifestations (50), but whether there are any long-term sequelae of GI involvement is unknown. Liver injury was common in SARS and MERS (51) and is also recognised with COVID-19; several studies have reported abnormal elevated liver enzymes in up to 53% of cases, and this correlated with more severe disease (50) .

Neurological sequelae appear in the literature as case reports and small case series and, as well as the recognised symptoms of headache, dizziness, encephalopathy and delirium, complications include acute stoke (Fig. 13) , Guillain-Barré syndrome, acute transverse myelitis, acute encephalitis, and posterior reversible encephalopathy syndrome (PRES; Fig. 14 ) (52) (53) (54) The pathophysiology of all these complications is not fully understood but is likely to be multifactorial. Whether they reflect the consequences of any severe viral illness, with associated inflammatory insult, together with the expected complications of any critical care admission, or are more specifically related to COVID-19 is yet to be Those who had a severe pneumonia will undergo a telephone clinical consultation 4-6 weeks post-discharge with CXR and face-to-face consultation at 12 weeks. For those with mild-moderate pneumonia, the telephone consultation can occur slightly later at 12 weeks post-discharge, together with a CXR.

Irrespective of the above advice, if lung malignancy is suspected, either an early repeat CXR 6 weeks after discharge or referral to local cancer services is advised; however, individual hospitals may adapt their own recall and urgent cancer pathways to suit, tailoring the timing of further investigation on an individualised basis according to the level of suspicion and physiological impairment. Importantly, follow-up CXR is not required in patients without radiological evidence of pneumonia, or in those whose radiological changes have resolved by the time of discharge.

Progression to CT in either of group will be determined by clinical review, physiological impairment and CXR findings. If there are persistent CXR changes and/or evidence of physiological impairment, unenhanced CT and CT pulmonary angiography (PA) should be considered. The rationale for performing both unenhanced and contrast-enhanced imaging relates to the potential prevalence of thromboembolic disease in COVID-19 and the superior diagnostic quality of unenhanced inspiratory CT in ILD. Contrast enhancement of the lung parenchyma, together with an expiratory phase of imaging (often seen with non-breath hold rapid CTPA), can make the differentiation between true and artefactual GGO challenging, particularly posteriorly at the bases, areas commonly involved in COVID-19 (2) (Fig.   15 ).

The reliance on imaging at 12 weeks post-discharge would suggest that a standardised template reporting system for CXR and CT could add significant benefit in post-COVID-19 follow-up and provide consistency for both community and hospital clinicians in terms of managing complications, as well as providing an opportunity for efficient long-term data collection.

In early March 2020, BSTI developed a simple, internationally recognised CXR reporting template for index COVID-19 presentation to help facilitate standardised reporting. This had embedded CXR reporting codes allowing retrospective radiology information (RIS) system keyword searches for audit purposes (1).

This new template is tailored for a post-COVID-19 CXR follow-up at 12 weeks and stratifies patients into one of five groups based on CXR findings: resolved (PCVCX0); significantly improved (PCVCX1); stable (PCVCX2); worsening, for example development of fibrosis even if alveolar opacity has improved ( Fig. 16; PCVCX3) , and other findings, for example, lung malignancy, pneumothorax, or new infection (PCVCX4).

Material Appendix S3)

The BSTI suggests similarly themed reporting codes for CT follow-up: normal (PCVCT0); improving (PCVCT1); stable (PCVCT2); fibrosis (PCVCT3), and other findings, similar to above (PCVCT4; Fig. 17 ). An additional PE code can also be incorporated: no PE (PCVPE0); new acute PE (PCVPE1); chronic PE (PVCPE2); for example, PCVCT1 + PCVPE1 would indicate resolving COVID-19 changes with new acute PE. Fig. 18 illustrates another example of the application of several of these RIS codes.

We are aware that many departments have rationalised imaging across all subspecialties within radiology during the COVID-19 pandemic. Routine imaging services were temporarily suspended and subspecialties have adjusted guidelines to manage the demand and pressures for imaging locally; however, given the relatively rapid median growth rates of lung cancer, nodule surveillance should be appropriately prioritised. Expert consensus broadly recommends that during the pandemic, the initial intended point of surveillance could be deferred by 3 to 6 months where the risk of malignancy is low (e.g., for a solid nodule sub-8 mm in J o u r n a l P r e -p r o o f diameter) (58) . It would thus seem pragmatic to perform surveillance CT as close as possible to intended time points, while deferring nodules where stability has already been demonstrated. For example, a nodule requiring 3-month surveillance CT, which has now been delayed by another 6 months (i.e., 9 months from baseline) should be performed immediately. If stable, current recommendations (59) would suggest performing the next follow-up at 12 months from baseline; however, this would then be only 3 months from the most recent CT. A multidisciplinary team may consider it appropriate and pragmatic to perform such a follow-up at a later time interval to allow for a longer duration over which to assess stability. We must stress that such approaches are currently not evidenced based, but may help to judiciously reduce a small percentage of potentially unnecessary examinations. In the recovery phase post-COVID-19, even such a modest reduction is vital.

As follow-up imaging will mostly be performed at 12 weeks, it would seem unlikely there will be active shedding of the virus at this time. Imaging should therefore ideally be performed at designated clean sites/scanners. Nevertheless, it should be noted that, as yet, there is no formal evidence stating that re-infection is unlikely, and it remains unclear how long any acquired immunity to SARS-CoV-2 will last.

Post-COVID-19 follow-up could generate a significant volume of new radiology workload in departments that are already stretched with capacity issues and significant backlogs. Radiology departments will also need to retain the flexibility to juggle workflow at short notice to cope with any future surges in infection including a potential second peak of the pandemic.

Given the sheer number of patients that have experienced severe lung damage from COVID-19, chronic pulmonary morbidity is likely to be one of the major lasting impacts on our healthcare system. Therapeutic trials of anti-fibrotic medication in COVID-19 are being constructed. It is hoped that automated image analysis tools combined with data science applied to health records will be able to identify patients at risk of pulmonary complications at an early stage and enable recruitment into clinical trials.

Given the interdependence of cardiac disease on lung health and lung disease on cardiac health, and the effects of both on neurological disease, the long-term health consequences for COVID-19 patients will necessitate close surveillance and reporting to national registries. To this end, imaging repositories such as the National COVID-19 chest imaging database (60) could provide a valuable resource that identifies healthcare needs and enables prioritisation of resources as the pandemic begins to stabilise (61). In the UK, the PHOSP-COVID study (62) is also standardising outpatient CT acquisition protocols in patients that had been admitted acutely for COVID-19. In particular, the PHOSP-COVID study (62) should allow a comprehensive evaluation of the prevalence and impact of COVID-19 on lung parenchymal, airway and vascular damage, as well as determining the effects of COVID-19 across various organ systems.

As the coronavirus pandemic begins to mature, the focus of imaging departments in the UK is changing direction to encompass the re-initiation of elective work whilst beginning to engage in the follow-up of patients previously diagnosed with COVID-19. Over the last 3 months, the multisystem effects of this disease have been recognised and, although comprehensive knowledge of their pathophysiology is still J o u r n a l P r e -p r o o f being sought, the need for a holistic approach to ongoing patient management and rehabilitation is acknowledged.

Thromboembolic complications and lung parenchymal damage are likely to be the commonest clinically significant sequelae in survivors of COVID-19. Although the epidemiology of pulmonary fibrosis has been inferred from previous SARS and MERS epidemics, the actual impact and prevalence of such complications will only be truly defined in the coming months.

Radiologists should be aware of the guidelines and imaging techniques for follow-up of patients with ongoing respiratory morbidity and such follow-up is likely to have an impact on service demand, stretching capacity further.

Standardised reporting templates and RIS codes can provide an element of consistency for clinicians involved in ongoing patient management and provide an opportunity for robust data collection.

Although there are specific guidelines for the follow-up of thoracic complications, patients with pulmonary fibrosis and pulmonary vascular disease (with or without pulmonary hypertension) will likely ultimately feed into existing clinicoradiological services, particularly with respect to the hub-and-spoke model for UK tertiary interstitial lung disease and pulmonary hypertension services.

Our knowledge of COVID-19 is changing at such a rate that speculation on its longterm impacts and relevant clinical questions may well be outdated by the time a manuscript goes to press, and there is also potential for the trajectory of this coronavirus pandemic to have changed within that timeframe. 

The continuing evolution of COVID-19 imaging pathways in the UK: a British Society of Thoracic Imaging Expert Reference Group update

An update on COVID-19 for the radiologist -a British Society of Thoracic Imaging Statement

Impact of severe acute respiratory syndrome (SARS) on pulmonary function, functional capacity and quality of life in a cohort of survivors

Follow-up chest radiographic findings in patients with MERS-CoV after recovery

Incidence of thrombotic complications in critically ill ICU patients with COVID-19

Acute pulmonary embolism and COVID-19 pneumonia: a random association?

Coronavirus disease 2019 (COVID-19): a systematic review of imaging findings in 919 patients

Acute respiratory failure in COVID-19: is it "typical

Clinical, laboratory and imaging features of COVID-19: a systematic review and metaanalysis

Epidemiology, microbiology and treatment considerations for bacterial pneumonia complicating influenza

Recognition and management of respiratory coinfection and secondary bacterial pneumonia in patients with COVID-19

Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study

Emergency tracheal intubation in 202 patients with COVID-19 in Wuhan, China: lessons learnt and international expert recommendations

Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study

Iatrogenic pneumothorax related to mechanical ventilation

Spontaneous pneumomediastinum: a probable unusual complication of coronavirus disease 2019 (COVID-19) pneumonia

Clinicopathology of severe acute respiratory syndrome: an autopsy case report

Autopsy findings and venous thromboembolism in patients with COVID-19. A prospective study

COVID-19 and its implications for thrombosis and anticoagulation

Hypoxaemia related to COVID-19:vascular and perfusion abnormalities on dual-energy CT

An epidemiological analysis of the burden of chronic thromboembolic pulmonary hypertension in the USA

CT measurement of central pulmonary arteries to diagnose pulmonary hypertension (PHTN): more reliable than valid?

Evaluation of the CT imaging findings in patients newly diagnosed with chronic thromboembolic pulmonary hypertension

Predictors of pulmonary hypertension on high-resolution conputed tomography of the chest in systemic sclerosis: a retrospective analysis

Detection of pulmonary hypertension with multidetector CT and echocardiography alone and in combination

Right ventricular to left ventricular ratio at CT pulmonary angiogram predicts mortality in interstitial lung disease

Predictive value of computed tomography in acute pulmonary embolism: systematic review and meta-analysis

The dilatation of main pulmonary artery and right ventricle observed by enhanced chest computed tomography predict poor outcome in inoperable chronic thromboembolic disease

Know the score. A review of the quality of care provided to patients aged over 16 years with a new diagnosis of pulmonary embolism. National Confidential Enquiry into Patient Outcome and Death

Diagnosis of chronic thromboembolic pulmonary hypertension

Analysis of thin-section CT in patients with coronavirus disease (COVID-19) after hospital discharge

Organising pneumonia: perilobular pattern at thin-section CT

Computed tomography findings in acute exacerbation of idiopathic pulmonary fibrosis

Imaging of pulmonary involvement in rheumatic disease

Review of the clinical characteristics of coronavirus disease 2019 (COVID-19)

Cardiovascular implications of fatal outcomes of patients with coronavirus disease 2019 (COVID-19)

Association of cardiac injury with mortality in hospitalised patients with COVID-19 in Wuhan, China

Neurological manifestations of hospitalised patients with COVID-19 in Wuhan, China: a retrospective case series study

Myocardial injury and COVID-19: possible mechanisms

Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China

Clinical characteristics of 138 hospitalised patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China

The variety of cardiovascular presentations of COVID-19

Myocarditis revealing COVID-19 infection in a young patient

COVID-19 and cardiovascular disease

Cardiac involvement in recovered COVID-19 patients identified by magnetic resonance imaging

SARS-CoV-2-induced Kawasaki-like hyperinflammatory syndrome: a novel COVID phenotype in children

COVID-19 and Kawasaki disease: novel virus and novel case

COVID-19 and Kawasaki disease: finding the signal in the noise

Kidney disease is associated with in-hospital death of patients with COVID-19

Gastrointestinal and liver manifestations in patients with COVID-19

Liver injury during highly pathogenic human coronavirus infections

Neurological manifestations and complications of COVID-19: a literature review

Posterior reversible encephalopathy syndrome (PRES) as a neurological association in severe COVID-19

Transient cortical blindness in COVID-19 pneumonia; a PRES-like syndrome: case report

COVID-19 infection and circulation ACE2 levels: protective role in women and children. Front Pediatr

Organ-protective effect of angiotensin-converting enzyme 2 and its effect on the prognosis of COVID-19

Respiratory follow-up of patients with COVID-19 pneumonia

Management of lung nodules and lung cancer screening during the COVID-19 pandemic

Akram AR on behalf of the British Thoracic Society Standards of Care Committee et al. British Thoracic Society Guidelines for the investigation and management of pulmonary nodules: accredited by NICE

J o u r n a l P r e -p r o o f 62. NIHR. Major study into long-term health effects of COVID-19 launched in the UK.