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Health care delivery, economics and global health care
Original research
Impact of COVID-19 on the imaging diagnosis of cardiac disease in Europe
  1. Michelle Claire Williams1,
  2. Leslee Shaw2,
  3. Cole B Hirschfeld3,
  4. Pal Maurovich-Horvat4,
  5. Bjarne L Nørgaard5,
  6. Gianluca Pontone6,
  7. Amelia Jimenez-Heffernan7,
  8. Valentin Sinitsyn8,
  9. Vladimir Sergienko9,
  10. Alexey Ansheles9,
  11. Jeroen J Bax10,
  12. Ronny Buechel11,
  13. Elisa Milan12,
  14. Riemer H J A Slart13,
  15. Edward Nicol14,
  16. Chiara Bucciarelli-Ducci15,16,
  17. Yaroslav Pynda17,
  18. Nathan Better18,
  19. Rodrigo Cerci19,
  20. Sharmila Dorbala20,
  21. Paolo Raggi21,
  22. Todd C Villines22,
  23. Joao Vitola19,
  24. Eli Malkovskiy3,
  25. Benjamin Goebel23,
  26. Yosef Cohen24,
  27. Michael Randazzo3,
  28. Thomas N B Pascual25,
  29. Maurizio Dondi17,
  30. Diana Paez17 and
  31. Andrew J Einstein26
  32. On behalf of INCAPS COVID Investigators Group
  1. 1 Centre for Cardiovascular Science, University of Edinburgh, Edinburgh, UK
  2. 2 Presbyterian Hospital/Weill Cornell Medical Center, New York, New York, USA
  3. 3 Columbia University Irving Medical Center, New York, New York, USA
  4. 4 MTA-SE Cardiovascular Imaging Research Group, Semmelweis University, Heart and Vascular Center, Budapest, Hungary
  5. 5 Cardiology, Aarhus University Hospital, Aarhus, Denmark
  6. 6 Department of Cardiovascular Imaging, Centro Cardiologico Monzino IRCCS, Milan, Italy
  7. 7 Hospital Juan Ramón Jiménez, Huelva, Spain
  8. 8 Lomonosov Moscow State University, Moscow, Russian Federation
  9. 9 National Medical Research Center of Cardiology of Healthcare Ministry, Moscow, Russian Federation
  10. 10 Department of Cardiology, Leiden University Medical Center, Leiden, The Netherlands
  11. 11 Department of Nuclear Medicine, University Hospital Zurich, Zurich, Switzerland
  12. 12 UOC Nuclear Medicine- Ospedale Cà Foncello, Treviso, Italy
  13. 13 Department of Nuclear Medicine and Molecular Imaging, University of Groningen, Groningen, The Netherlands
  14. 14 Department of Imaging, Royal Brompton Hospital, London, UK
  15. 15 Royal Brompton and Harefield Hospitals, London, UK
  16. 16 Guys and St Thomas NHS Trust and King’s College London, London, UK
  17. 17 International Atomic Energy Agency, Vienna, Austria
  18. 18 Royal Melbourne Hospital and University of Melbourne, Melbourne, Victoria, Australia
  19. 19 Quanta Diagnostico, Curitiba, Brazil
  20. 20 Brigham and Women's Hospital, Boston, Massachusetts, USA
  21. 21 Division of Cardiology, University of Alberta, Edmonton, Alberta, Canada
  22. 22 Medicine (Cardiology), Walter Reed National Military Medical Center, Bethesda, Maryland, USA
  23. 23 Weill Cornell Medical College, New York, New York, USA
  24. 24 Technion Israel Institute of Technology, Haifa, Israel
  25. 25 Philippine Nuclear Research Institute, Quezon City, Philippines
  26. 26 Columbia University Medical Center, New York, New York, USA
  1. Correspondence to Dr Michelle Claire Williams; michelle.williams{at}ed.ac.uk

Abstract

Objectives We aimed to explore the impact of the COVID-19 pandemic on cardiac diagnostic testing and practice and to assess its impact in different regions in Europe.

Methods The online survey organised by the International Atomic Energy Agency Division of Human Health collected information on changes in cardiac imaging procedural volumes between March 2019 and March/April 2020. Data were collected from 909 centres in 108 countries.

Results Centres in Northern and Southern Europe were more likely to cancel all outpatient activities compared with Western and Eastern Europe. There was a greater reduction in total procedure volumes in Europe compared with the rest of the world in March 2020 (45% vs 41%, p=0.003), with a more marked reduction in Southern Europe (58%), but by April 2020 this was similar in Europe and the rest of the world (69% vs 63%, p=0.261). Regional variations were apparent between imaging modalities, but the largest reductions were in Southern Europe for nearly all modalities. In March 2020, location in Southern Europe was the only independent predictor of the reduction in procedure volume. However, in April 2020, lower gross domestic product and higher COVID-19 deaths were the only independent predictors.

Conclusion The first wave of the COVID-19 pandemic had a significant impact on care of patients with cardiac disease, with substantial regional variations in Europe. This has potential long-term implications for patients and plans are required to enable the diagnosis of non-COVID-19 conditions during the ongoing pandemic.

  • COVID-19
  • cardiac imaging techniques
  • coronary artery disease

Data availability statement

No data are available. As data were provided in confidence to the IAEA by survey respondents, sharing of the underlying data is not possible.

http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

https://doi.org/10.1136/openhrt-2021-001681

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    Key questions

    What is already known about this subject?

    • Worldwide COVID-19 has had a dramatic impact on care of patients with cardiovascular disease. However, the impact on cardiac diagnostic testing in Europe has not been studied.

    What does this study add?

    • The COVID-19 pandemic resulted in a reduction in cardiac imaging in Europe of 45% in March 2020 and 69% in April 2020 compared with 2019, with the largest reduction in Southern Europe. In April 2020, lower gross domestic product and higher COVID-19 deaths were independent predictors of the reduction in cardiac imaging.

    How might this impact on clinical practice?

    • The considerable variability in the response to the pandemic has important implications for patient care. It is important to identify patients who have missed out on diagnostic testing. In addition, preparation for future waves of the pandemic should address these issues.

    Introduction

    Non-communicable diseases, including cardiovascular disease, remain the leading cause of mortality around the world. However, during the COVID-19 pandemic, there has been a dramatic disruption in healthcare provision around the world. Accurate diagnosis is central to the treatment of cardiac disease and delayed or missed diagnoses have the potential to impact long-term morbidity and mortality. After China and some countries in Southeast Asia, Europe became the epicentre of COVID-19 in March 2020. This paper focuses on the impact of the first peak of the COVID-19 pandemic on the management of cardiac disease in Europe compared with the rest of the world, in order to provide important learning opportunities for impending waves of the COVID-19 pandemic and for future pandemics.

    Established guidelines have been developed which place non-invasive imaging at the centre of the diagnosis and management of coronary artery disease. However, during the COVID-19 pandemic, both guidelines1–5 and local practices have changed. We have recently shown in an international survey that the COVID-19 pandemic was associated with a significant reduction in cardiac imaging around the world, with a 64% reduction in cardiac imaging between March 2019 and April 2020.6 Several studies have shown that during the March/April 2020 COVID-19 peak, there was a reduction in hospital admissions for acute coronary syndromes,7–9 and an increase in out-of-hospital cardiac arrests10 with excess cardiovascular mortality around the world.11 Furthermore, COVID-19 is itself potentially associated with myocardial injury, arrhythmia, and venous and arterial thrombosis.12 13 It is therefore essential that the diagnosis and management of cardiac disease is optimised during the COVID-19 pandemic.

    The International Atomic Energy Agency (IAEA) Division of Human Health aims to support member states to combat cardiovascular diseases, cancer, malnutrition and other diseases through the use of appropriate prevention, diagnostic testing and treatment. In this light, the IAEA coordinated a worldwide survey of cardiac imaging laboratories (the IAEA Noninvasive Cardiology Protocols Study of COVID-19, INCAPS COVID Survey), to assess the impact of the pandemic on the diagnosis of cardiac disease. This analysis of the INCAPS COVID Survey aims to assess the impact of the COVID-19 pandemic on the diagnosis of cardiac diseases in Europe during the first peak of the pandemic, in order to inform future strategies.

    Methods

    Study design

    Data for this study were collected as part of the IAEA survey on the impact of COVID-19 on cardiac imaging (INCAPS COVID). An online survey was developed by a steering committee which included experts in cardiology and cardiovascular imaging. The survey included questions regarding the healthcare facility, healthcare professionals, personal protective equipment, strategic plans for reopening and changes in procedural volumes for a range of cardiac imaging procedures.

    Data collection

    Survey data were collected using a secure software platform used by the IAEA, the International Research Integration System (https://iris.iaea.org). Participation was encouraged using email and social media activity, from the IAEA, national and international cardiology and imaging societies and from national coordinators. No patient-specific or confidential data were collected. Patients or the public were not involved in the design, conduct, reporting or dissemination plans of this publication. During data collection, the Data Coordination Committee reviewed entries and reached out to survey participants with questions regarding missing, implausible, duplicate or inconsistent data. Participants were provided the opportunity to clarify and correct response as needed. For each centre, only one entry was included in the final dataset. Final database cleaning was completed on 1 July 2020. Entries were excluded for reasons such as missing or incomplete responses to the questionnaire. As data were provided in confidence to the IAEA by survey respondents, sharing of the underlying data is not possible.

    Population data were based on data obtained from World Bank from 2019.14 Data on COVID-19 cases and deaths in March and April 2020 were obtained from the WHO COVID-19 dashboard.15 Territories were not included in per country COVID-19 case numbers. Information on gross domestic product (GDP) was obtained from the World Bank for 2019.14 Income group was defined using the World Bank classification of high, upper-middle, lower-middle and low.16

    Cardiac imaging procedure volumes

    Participants were asked to provide estimates of procedure volumes from March 2019, March 2020 and April 2020, including both anatomical and functional imaging. Anatomical imaging included transthoracic echocardiography (TTE), transoesophageal echocardiography (TOE), cardiac magnetic resonance (CMR, non-stress), positron emission tomography (PET) infection studies, coronary artery calcium scanning, coronary CT angiography (CCTA) and invasive coronary angiography (ICA). Functional imaging included stress ECG, stress echocardiography, stress single-photon emission CT (SPECT), stress PET and stress CMR. Stress nuclear imaging included combined data from stress SPECT and stress PET. Data were aggregated on a regional level. Countries in Europe were defined using the United Nations geoscheme.17 European countries were divided into Northern, Southern, Eastern and Western regions, with Turkey and Cyprus included in the Eastern region.

    Statistical analysis

    In total, 936 questionnaires were submitted, and 27 duplicates were excluded from the results. Statistical analysis was performed using R (V.4.0.1, R Development Core Team, Vienna, Austria). Survey question responses are presented as number and percentage. Continuous data that are not normally distributed are presented as median and interquartile interval. Percentage change in procedure volume was compared between March 2019 and March or April 2020. A linear regression model was constructed to assess the impact of European region, population, GDP and COVID-19 deaths at a country level, on procedure volume reduction at a centre level in March and April 2020 compared with March 2019. COVID-19 cases and COVID-19 deaths were strongly correlated on a per country basis, but as the availability of COVID-19 testing was variable across countries, particularly in the early stages of the pandemic, COVID-19 deaths were chosen for inclusion in the linear regression model. Population, GDP and COVID-19 deaths were log transformed for analysis.

    Results

    Centres

    Around the world data were collected from 909 centres in 108 countries, and of these 845 centres in 106 countries provided data on procedure volumes. In Europe, data were collected from 241 centres in 40 countries, including 38 (16%) centres in Western Europe, 95 (39%) in Southern Europe, 38 (16%) in Eastern Europe and 70 (29%) in Northern Europe (table 1). Compared with the rest of the world, European centres were more likely to have inpatient facilities (95% vs 76%, p<0.001), teaching facilities (80% vs 61%, p<0.001) and had more hospital beds (700 (IQI 345–999) vs 450 (IQI 200–800), p<0.001; table 1). The number of hospital beds per centre was largest in Western Europe (table 1, p=0.034), but there were no other differences in facility type between European regions.

    View this table:
    Table 1

    Information on centres providing data for the survey in different European regions and comparisons between Europe and the rest of the world

    Changes to imaging procedure volumes

    In surveyed European centres, a total of 142 463 procedures were performed in March 2019. There was a 45% reduction in total procedure volume in March 2020 (n=78 969) and a 69% reduction in April 2020 (n=44 469). For functional imaging in Europe in April 2020, the largest reductions in procedure volume compared with March 2019 were identified in stress echocardiography (84%), followed by stress ECG (83%), stress SPECT (79%), stress CMR (68%) and stress PET (42%, table 2). For anatomical imaging in Europe in April 2020 compared with March 2019, reductions in procedures by modality were identified in CT calcium score (78%), followed by TEE (74%), CMR (non-stress, 72%), CCTA (69%), TTE (67%), PET studies for infection (53%) and ICA (51%, table 2). In April 2020, procedure volume reductions were similar in Europe compared with the rest of the world for all modalities, except for larger reductions in stress SPECT (79% vs 73%, p=0.002), stress nuclear (77% vs 72%, p=0.012) and CCTA (69% vs 50%, p=0.003, table 2).

    View this table:
    Table 2

    Reduction in procedure volumes across European regions compared with the rest of the world

    There were regional and country variations in the reduction in total procedures (figure 1). In March 2020, there was a larger reduction in total procedures in Europe compared with the rest of the world (45% vs 41%, p=0.003), with the largest reductions in Southern Europe (58%, p<0.001, table 2). In April 2020, the reduction in total procedures was similar in Europe and the rest of the world (69% vs 63%, p=0.261), and Southern Europe remained the region with the highest total procedure reduction (78%, p<0.001).

    Figure 1
    Figure 1

    Reduction in total cardiac imaging procedure volume (March 2019–March 2020 and March 2019–April 2020).

    For all modalities, the reduction in procedure volume was higher in April 2020 compared with March 2020 (figures 2 and 3). Regional variations were apparent with the largest reductions in Southern Europe in both March and April 2020 for all modalities apart from CT calcium score, stress echocardiography and PET infection studies. In April 2020, procedure volume reductions were highest in Southern Europe for stress PET (94% reduction, p=0.006), stress nuclear (84% reduction, p=0.014), CMR (non-stress, 78% reduction, p=0.010) and invasive coronary angiography (63% reduction, p=0.009, table 2). Reduction in PET infection studies was highest in Eastern Europe (71% and 92%, respectively, p<0.001). Reductions in stress CMR and non-stress CMR were highest in Southern and Northern Europe (table 2).

    Figure 2
    Figure 2

    Reduction in procedure volume for functional imaging in different regions of Europe from March 2019 to March 2020 and April 2020. CMR, cardiac magnetic resonance.

    Figure 3
    Figure 3

    Reduction in procedure volume for anatomical imaging in different regions of Europe from March 2019 to March 2020 and April 2020. CCTA, coronary CT angiography; CMR, cardiac magnetic resonance (non-stress); TEE, transoesophageal echocardiography; TTE, transthoracic echocardiography.

    During March and April 2020, there were 1 406 184 COVID-19 cases recorded in European countries represented in the survey, with more occurring in Western and Southern Europe compared with Northern or Eastern Europe (table 1). When centres providing information were stratified by World Bank income group, there were 210 European centres located in high-income countries, 29 in upper middle-income countries and 2 in low/middle-income countries. In April 2020, the European reduction in procedure volumes was highest in Europe in upper middle-income countries (77%), compared with high-income countries (68%) and lower middle-income countries (36%, p=0.017). Multivariable analysis showed that in March 2020, location in Southern Europe was the only independent predictor of a reduction in cardiac imaging procedure volume (figure 4). However, in April 2020, multivariable analysis showed that lower GDP and higher COVID-19 deaths were the only independent predictors of a reduction in imaging procedure volume (figure 4).

    Figure 4
    Figure 4

    Multivariable models for the reduction in procedure volume at centres from March 2019 to (A) March 2020 and (B) April 2020. Population, GDP and COVID-19 deaths were log transformed for analysis (log10). Graphs show estimate of the beta coefficients and SE. * indicates a p value of <0.05. European regions were compared with Western Europe as the baseline. GDP, gross domestic product.

    Changes in practice, imaging protocols and staffing

    In Europe, 85% of centres reduced outpatient activities during March/April 2020, while 44% of centres cancelled all outpatient activities, similar to the rest of the world (table 3). Among European regions, the proportion of centres cancelling all outpatient activities was lower in Eastern and Western Europe compared with the other regions. European centres were also more likely to be planning phased reopening compared with the rest of the world (58% vs 51%, p=0.003), and this was particularly common in Western Europe (85%, p=0.001).

    View this table:
    Table 3

    Imaging departments’ change in capacity and practice

    European centres were more likely to use extended working hours but less likely to use telehealth and remote reporting, compared with the rest of the world (table 2). Within Europe, the use of remote reporting was more common in Western and Northern Europe. European centres were less likely to perform temperature measurements, symptom screening and COVID-19 testing in imaging centres compared with the rest of the world. There were regional variations in the planning of patient arrivals, physical distancing in waiting areas, separate spaces for patients with COVID-19, limiting visitors, use of temperature measurements, masks for patients/visitors and increasing time for cleaning. European centres were less likely to change imaging protocols compared with the rest of the world (table 4), with regional variations in the use of exercise stress and modifications to cardiac nuclear and CT protocols. Redeployment of imaging staff was less frequent in Europe compared with the rest of the world (15% vs 22%, p=0.011). Use of furlough, reducing salaries or laying off staff was less frequent in Europe compared with the rest of the world (table 4).

    View this table:
    Table 4

    Imaging departments’ change in imaging protocols and staffing

    Discussion

    The COVID-19 pandemic has had a dramatic impact on the provision of healthcare around the world. In this international survey of 108 countries, we have shown the substantial impact of the COVID-19 pandemic on the care of patients with cardiac disease. Responses to the COVID-19 pandemic varied throughout European countries and European regions, with a 45% reduction in total cardiac imaging in March 2020 and a 69% reduction in April 2020. Reductions in cardiac imaging and changes to practices were greater in Europe compared with the rest of the world, particularly in Southern Europe, reflecting the trajectory of the pandemic at the time of the survey. Only location in Southern Europe was a predictor of the reduction of cardiac imaging in March 2020, whereas lower GDP and higher COVID-19 deaths were independent predictors in April 2020. This highlights the considerable variability in the response to the pandemic, which has important implications for patient care.

    Cardiac imaging is central to the diagnostic pathway for many patients, with both acute and chronic conditions. Without accurate diagnoses, appropriate treatment cannot be provided. The COVID-19 pandemic has caused both delay and complete inability to obtain a diagnosis for many patients with cardiac conditions around the world. In Europe, in particular, only half the usual number of procedures were performed in March 2020, and one-third in April 2020. This may have important short-term and long-term health implications. In addition, patients with underlying cardiovascular disease are at an increased risk of poor outcomes following COVID-19 infection.18–21

    During the COVID-19 pandemic, several studies have reported an increase in out-of-hospital cardiac arrests10 22 and excess cardiovascular mortality.11 In March 2020, there was a 48% reduction in admissions with acute myocardial infarction to Italian coronary care units23 and in April 2020, there was a 52% increase in out-of-hospital cardiac arrests in some regions in Italy.22 Similarly, in England in March 2020, there was a 40% reduction in hospital admissions for acute coronary syndromes compared with the previous year.7 The worldwide reduction in hospital admissions with acute coronary syndromes7–9 23–25 is particularly concerning, as rapid diagnosis and treatment of this condition has been responsible for significant improvements in morbidity and mortality in recent years. Delays in cardiac diagnostic imaging may also impact other cardiovascular treatments such as transcatheter aortic valve implantation26 and cardiac surgery.27

    The long-term implications of delays in making an accurate diagnosis of cardiac diseases are currently uncertain, but our survey shows that there are many thousands of patients who have had their diagnosis delayed or prevented. It is possible that we may see later presentations or more severe presentations of cardiac conditions. Over the longer term, these patients may not be receiving appropriate preventative treatments because of their delayed diagnosis, and this may have downstream implications on cardiac morbidity and mortality. Guidelines have been developed to aid with the restarting of cardiac imaging services.1 2 5 28 29 Addressing this issue in a timely manner will be an important issue for health policymakers as countries deal with future waves of the COVID-19 pandemic and subsequent recovery.

    Responses to the COVID-19 pandemic have varied between and within countries throughout Europe, influenced by a variety of factors including COVID-19 case numbers, the underlying healthcare system and political factors. We have shown that there were patterns in the application of these policies for healthcare in different regions in Europe, which initially reflected regional location but by April 2020 reflected COVID-19 deaths and GDP. Countries with a lower GDP were more likely to reduce cardiac imaging procedures in April 2020, likely in an attempt to prevent their healthcare systems becoming overwhelmed. In addition to policies cancelling non-urgent investigations, other important factors may have driven the decline in performance of imaging procedures, such as patient’s inability or reluctance to seek healthcare advice during the COVID-19 pandemic. This includes factors such as fear, a desire to avoid potential infection, access to public transport and other essential axillary services. This appears to be part of a general pattern of reduced healthcare utility for non-COVID-19 conditions during the pandemic. For example, emergency department visits decreased 41%–64% in the USA30 and delayed cancer diagnoses are predicted to result in a significant increase in mortality over the next 5 years.31 It is therefore essential that we optimise healthcare access for patients with non-COVID-19 conditions during the pandemic.

    This was a self-reported survey and thus has some limitations. Efforts were made to distribute this survey widely, but we cannot exclude that the included sites represent outliers in each country. Sampling and response bias are a potential issue with these data, as with any survey. This analysis was not based on national reporting of procedure numbers which may have been more thorough in some countries, but is not available or is inconsistent in many countries around the world. Country-level data for income and COVID-19 cases and deaths were used rather than centre-level data. Information for this survey was obtained during March and April 2020, which represented the initial peak of the COVID-19 pandemic in some countries. However, for some countries around the world, the peak came later, and for China the peak came earlier. We plan further surveys to assess further changes in practice. We found that in Europe, the reduction in procedure volumes was highest in upper middle-income countries compared with high or lower middle-income countries, which is different from the pattern observed worldwide.6 This may reflect the small number of lower middle-income European countries included in this survey and the distribution of countries of different income groups relative to the geographical epicentres of the early pandemic. In addition, country-based variations in the recording of COVID-19 cases and deaths may impact results.

    In conclusion, we have shown the significant impact of the COVID-19 pandemic on the performance of diagnostic imaging for cardiac disease in Europe. This survey provides important information, as we now need to learn how to deal with an ongoing viral pandemic at the same time as managing patients with cardiac diseases.

    Supplemental material

    Data availability statement

    No data are available. As data were provided in confidence to the IAEA by survey respondents, sharing of the underlying data is not possible.

    Ethics statements

    Ethics approval

    All participation by study sites was voluntary and no patient-level data were provided, therefore it was deemed that no external ethics committee review was required.

    Acknowledgments

    The INCAPS COVID Investigators Group, listed by name in the online supplemental information, thank cardiology and imaging professional societies worldwide for their assistance in disseminating the survey to their memberships. These include alphabetically, but are not limited to: American Society of Nuclear Cardiology, Arab Society of Nuclear Medicine, Australasian Association of Nuclear Medicine Specialists, Australia-New Zealand Society of Nuclear Medicine, Belgian Society of Nuclear Medicine, Brazilian Nuclear Medicine Society, British Society of Cardiovascular Imaging, Conjoint Committee for the Recognition of Training in CT Coronary Angiography (Australia and New Zealand), Consortium of Universities and Institutions in Japan, Gruppo Italiano Cardiologia Nucleare, The Danish Society of Cardiology, Sociedad Española de Medicina Nuclear e Imagen Molecular, Indonesian Society of Nuclear Medicine, Japanese Society of Nuclear Cardiology, Philippine Society of Nuclear Medicine, Russian Society of Radiology, Moscow Regional Department of Russian Nuclear Medicine Society, Society of Cardiovascular Computed Tomography, and Thailand Society of Nuclear Medicine. MCW (FS/ICRF/20/26002) is supported by the British Heart Foundation.

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    Footnotes

    • Twitter @imagingmedsci, @chiarabd

    • Collaborators INCAPS COVID Investigators Group: Mohammad Nawaz Nasery; Artan Goda; Ervina Shirka; Rabie Benlabgaa; Salah Bouyoucef; Abdelkader Medjahedi; Qais Nailli; Mariela Agolti; Roberto Nicolas Aguero; Maria del Carmen Alak; Lucia Graciela Alberguina; Guillermo Arroñada; Andrea Astesiano; Alfredo Astesiano; Carolina Bas Norton; Pablo Benteo; Juan Blanco; Juan Manuel Bonelli; Jose Javier Bustos; Raul Cabrejas; Jorge Cachero; Roxana Campisi; Alejandro Canderoli; Silvia Carames; Patrícia Carrascosa; Ricardo Castro; Oscar Cendoya; Luciano Martin Cognigni; Carlos Collaud; Carlos Collaud; Claudia Cortes; Javier Courtis; Daniel Cragnolino; Mariana Daicz; Alejandro De La Vega; Silvia Teresa De Maria; Horacio Del Riego; Fernando Dettori; Alejandro Deviggiano; Laura Dragonetti; Mario Embon; Ruben Emilio Enriquez; Jorge Ensinas; Fernando Faccio; Adolfo Facello; Diego Garofalo; Ricardo Geronazzo; Natalia Gonza; Lucas Gutierrez; Miguel Angel Guzzo; Miguel Angel Guzzo; Victor Hasbani; Melina Huerin; Victor Jäger; Julio Manuel Lewkowicz; Maria Nieves A López De Munaín; Jose Maria Lotti; Alejandra Marquez; Osvaldo Masoli; Osvaldo Horacio Masoli; Edgardo Mastrovito; Matias Mayoraz; Graciela Eva Melado; Anibal Mele; Maria Fernanda Merani; Alejandro Horacio Meretta; Susana Molteni; Marcos Montecinos; Eduardo Noguera; Carlos Novoa; Claudio Pereyra Sueldo; Sebastian Perez Ascani; Pablo Pollono; Maria Paula Pujol; Alejandro Radzinschi; Gustavo Raimondi; Marcela Redruello; Marina Rodríguez; Matías Rodríguez; Romina Lorena Romero; Arturo Romero Acuña; Federico Rovaletti; Lucas San Miguel; Lucrecia Solari; Bruno Strada; Sonia Traverso; Sonia Simona Traverzo; Maria del Huerto Velazquez Espeche; Juan Sebastian Weihmuller; Juan Wolcan; Susana Zeffiro; Mari Sakanyan; Scott Beuzeville; Raef Boktor; Patrick Butler; Jennifer Calcott; Loretta Carr; Virgil Chan; Charles Chao; Woon Chong; Mark Dobson; D’Arne Downie; Girish Dwivedi; Barry Elison; Jean Engela; Roslyn Francis; Anand Gaikwad; Ashok Gangasandra Basavaraj; Bruce Goodwin; Robert Greenough; Christian Hamilton-Craig; Victar Hsieh; Subodh Joshi; Karin Lederer; Kenneth Lee; Joseph Lee; John Magnussen; Nghi Mai; Gordon Mander; Fiona Murton; Dee Nandurkar; Johanne Neill; Edward O’Rourke; Patricia O’Sullivan; George Pandos; Kunthi Pathmaraj; Alexander Pitman; Rohan Poulter; Manuja Premaratne; David Prior; Lloyd Ridley; Natalie Rutherford; Hamid Salehi; Connor Saunders; Luke Scarlett; Sujith Seneviratne; Deepa Shetty; Ganesh Shrestha; Jonathan Shulman; Vijay Solanki; Tony Stanton; Murch Stuart; Michael Stubbs; Ian Swainson; Kim Taubman; Andrew Taylor; Paul Thomas; Steven Unger; Anthony Upton; Shankar Vamadevan; William Van Gaal; Johan Verjans; Demetrius Voutnis; Victor Wayne; Peter Wilson; David Wong; Kirby Wong; John Younger; Gudrun Feuchtner; Siroos Mirzaei; Konrad Weiss; Natallia Maroz-Vadalazhskaya; Olivier Gheysens; Filip Homans; Rodrigo Moreno-Reyes; Agnès Pasquet; Veronique Roelants; Caroline M. Van De Heyning; Raúl Araujo Ríos; Valentina Soldat-Stankovic; Sinisa Stankovic; Maria Helena Albernaz Siqueira; Augusto Almeida; Paulo Henrique Alves Togni; Jose Henrique Andrade; Luciana Andrade; Carlos Anselmi; Roberta Araújo; Guilherme Azevedo; Sabbrina Bezerra; Rodrigo Biancardi; Gabriel Blacher Grossman; Simone Brandão; Diego Bromfman Pianta; Lara Carreira; Bruno Castro; Tien Chang; Fernando Cunali Jr.; Roberto Cury; Roberto Dantas; Fernando de Amorim Fernandes; Andrea De Lorenzo; Robson De Macedo Filho; Fernanda Erthal; Fabio Fernandes; Juliano Fernandes; Fabio Fernandes; Thiago Ferreira De Souza; Wilson Furlan Alves; Bruno Ghini; Luiz Goncalves; Ilan Gottlieb; Marcelo Hadlich; Vinícius Kameoka; Ronaldo Lima; Adna Lima; Rafael Willain Lopes; Ricardo Machado e Silva; Tiago Magalhães; Fábio Martins Silva; Luiz Eduardo Mastrocola; Fábio Medeiros; José Claudio Meneghetti; Vania Naue; Danilo Naves; Roberto Nolasco; Cesar Nomura; Joao Bruno Oliveira; Eduardo Paixao; Filipe Penna De Carvalho; Ibraim Pinto; Priscila Possetti; Mayra Quinta; Rodrigo Rizzo Nogueira Ramos; Ricardo Rocha; Alfredo Rodrigues; Carlos Rodrigues; Leila Romantini; Adelina Sanches; Sara Santana; Leonardo Sara da Silva; Paulo Schvartzman; Cristina Sebastião Matushita; Tiago Senra; Afonso Shiozaki; Maria Eduarda Menezes de Siqueira; Cristiano Siqueira; Paola Smanio; Carlos Eduardo Soares; José Soares Junior; Marcio Sommer Bittencourt; Bernardo Spiro; Cláudio Tinoco Mesquita; Jorge Torreao; Rafael Torres; Marly Uellendahl; Guilherme Urpia Monte; Otávia Veríssimo; Estevan Vieira Cabeda; Felipe Villela Pedras; Roberto Waltrick; Marcello Zapparoli; Hamid Naseer; Marina Garcheva-Tsacheva; Irena Kostadinova; Youdaline Theng; Gad Abikhzer; Rene Barette; Benjamin Chow; Dominique Dabreo; Matthias Friedrich; Ria Garg; Mohammed Nassoh Hafez; Chris Johnson; Marla Kiess; Jonathon Leipsic; Eugene Leung; Robert Miller; Anastasia Oikonomou; Stephan Probst; Idan Roifman; Gary Small; Vikas Tandon; Adwait Trivedi; James White; Katherine Zukotynski; Jose Canessa; Gabriel Castro Muñoz; Carmen Concha; Pablo Hidalgo; Cesar Lovera; Teresa Massardo; Luis Salazar Vargas; Pedro Abad; Harold Arturo; Sandra Ayala; Luis Benitez; Alberto Cadena; Carlos Caicedo; Antonio Calderón Moncayo; Antonio Calderón Moncayo; Sharon Gomez; Claudia T. Gutierrez Villamil; Claudia Jaimes; Juan Londoño; Juan Luis Londoño Blair; Luz Pabon; Mauricio Pineda; Juan Carlos Rojas; Diego Ruiz; Manuel Valencia Escobar; Andres Vasquez; Damiana Vergel; Alejandro Zuluaga; Isabel Berrocal Gamboa; Gabriel Castro; Ulises González; Ana Baric; Tonci Batinic; Maja Franceschi; Maja Hrabak Paar; Mladen Jukic; Petar Medakovic; Viktor Persic; Marina Prpic; Ante Punda; Juan Felipe Batista; Juan Manuel Gómez Lauchy; Yamile Marcos Gutierrez; Yamile Marcos Gutierrez; Rayner Menéndez; Amalia Peix; Luis Rochela; Christoforos Panagidis; Ioannis Petrou; Vaclav Engelmann; Milan Kaminek; Vladimír Kincl; Otto Lang; Milan Simanek; Jawdat Abdulla; Morten Bøttcher; Mette Christensen; Lars Christian Gormsen; Philip Hasbak; Søren Hess; Paw Holdgaard; Allan Johansen; Kasper Kyhl; Bjarne Linde Norgaard; Kristian Altern Øvrehus; Niels Peter Rønnow Sand; Rolf Steffensen; Anders Thomassen; Bo Zerahn; Alfredo Perez; Giovanni Alejandro Escorza Velez; Mayra Sanchez Velez; Islam Shawky Abdel Aziz; Mahasen Abougabal; Taghreed Ahmed; Adel Allam; Ahmed Asfour; Mona Hassan; Alia Hassan; Ahmed Ibrahim; Sameh Kaffas; Ahmed Kandeel; Mohamed Mandour Ali; Ahmad Mansy; Hany Maurice; Sherif Nabil; Mahmoud Shaaban; Ana Camila Flores; Anne Poksi; Juhani Knuuti; Velipekka Kokkonen; Martti Larikka; Valtteri Uusitalo; Matthieu Bailly; Samuel Burg; Jean-François Deux; Vincent Habouzit; Fabien Hyafil; Olivier Lairez; Franck Proffit; Hamza Regaieg; Laure Sarda-Mantel; Vania Tacher; Roman P. Schneider; Harold Ayetey; George Angelidis; Aikaterini Archontaki; Sofia Chatziioannou; Ioannis Datseris; Christina Fragkaki; Panagiotis Georgoulias; Sophia Koukouraki; Maria Koutelou; Eleni Kyrozi; Evangelos Repasos; Petros Stavrou; Pipitsa Valsamaki; Carla Gonzalez; Goleat Gutierrez; Alejandro Maldonado; Klara Buga; Ildiko Garai; Pál Maurovich-Horvat; Erzsébet Schmidt; Balint Szilveszter; Edit Várady; Nilesh Banthia; Jinendra Kumar Bhagat; Rishi Bhargava; Vivek Bhat; Mona Bhatia; Partha Choudhury; Vijay Sai Chowdekar; Aparna Irodi; Shashank Jain; Elizabeth Joseph; Sukriti Kumar; Prof Dr Girijanandan Mahapatra; Deepanjan Mitra; Bhagwant Rai Mittal; Ahmad Ozair; Chetan Patel; Tapan Patel; Ravi Patel; Shivani Patel; Sudhir Saxena; Shantanu Sengupta; Santosh Singh; Bhanupriya Singh; Ashwani Sood; Atul Verma; Erwin Affandi; Padma Savenadia Alam; Edison Edison; Gani Gunawan; Habusari Hapkido; Basuki Hidayat; Aulia Huda; Anggoro Praja Mukti; Djoko Prawiro; Erwin Affandi Soeriadi; Hilman Syawaluddin; Amjed Albadr; Majid Assadi; Farshad Emami; Golnaz Houshmand; Majid Maleki; Maryam Tajik Rostami; Seyed Rasoul Zakavi; Eed Abu Zaid; Svetlana Agranovich; Yoav Arnson; Rachel Bar-Shalom; Alex Frenkel; Galit Knafo; Rachel Lugassi; Israel Shlomo Maor Moalem; Maya Mor; Noam Muskal; Sara Ranser; Aryeh Shalev; Domenico Albano; Pierpaolo Alongi; Gaspare Arnone; Elisa Bagatin; Sergio Baldari; Matteo Bauckneht; Paolo Bertelli; Francesco Bianco; Rachele Bonfiglioli; Roberto Boni; Andrea Bruno; Isabella Bruno; Elena Busnardo; Elena Califaretti; Luca Camoni; Aldo Carnevale; Roberta Casoni; Armando Ugo Cavallo; Giorgio Cavenaghi; Franca Chierichetti; Marcello Chiocchi; Corrado Cittanti; Mauro Colletta; Umberto Conti; Alberto Cossu; Alberto Cuocolo; Marco Cuzzocrea; Maria Luisa De Rimini; Giuseppe De Vincentis; Eleonora Del Giudice; Alberico Del Torto; Veronica Della Tommasina; Rexhep Durmo; Paola Anna Erba; Laura Evangelista; Riccardo Faletti; Evelina Faragasso; Mohsen Farsad; Paola Ferro; Luigia Florimonte; Viviana Frantellizzi; Fabio Massimo Fringuelli; Marco Gatti; Angela Gaudiano; Alessia Gimelli; Raffaele Giubbini; Francesca Giuffrida; Salvatore Ialuna; Riccardo Laudicella; Lucia Leccisotti; Lucia Leva; Riccardo Liga; Carlo Liguori; Giampiero Longo; Margherita Maffione; Maria Elisabetta Mancini; Claudio Marcassa; Elisa Milan; Barbara Nardi; Sara Pacella; Giovanna Pepe; Gianluca Pontone; Sabina Pulizzi; Natale Quartuccio; Lucia Rampin; Fabrizio Ricci; Pierluigi Rossini; Giuseppe Rubini; Vincenzo Russo; Gian Mauro Sacchetti; Gianmario Sambuceti; Massimo Scarano; Roberto Sciagrà; Massimiliano Sperandio; Antonella Stefanelli; Guido Ventroni; Stefania Zoboli; Dainia Baugh; Duane Chambers; Ernest Madu; Felix Nunura; Hiroshi Asano; Chimura Misato Chimura; Shinichiro Fujimoto; Koichiro Fujisue; Tomohisa Fukunaga; Yoshimitsu Fukushima; Kae Fukuyama; Jun Hashimoto; Yasutaka Ichikawa; Nobuo Iguchi; Masamichi Imai; Anri Inaki; Hayato Ishimura; Satoshi Isobe; Toshiaki Kadokami; Takao Kato; Takashi Kudo; Shinichiro Kumita; Hirotaka Maruno; Hiroyuki Mataki; Masao Miyagawa; Ryota Morimoto; Masao Moroi; Shigeki Nagamachi; Kenichi Nakajima; Tomoaki Nakata; Ryo Nakazato; Mamoru Nanasato; Masanao Naya; Takashi Norikane; Yasutoshi Ohta; Satoshi Okayama; Atsutaka Okizaki; Yoichi Otomi; Hideki Otsuka; Masaki Saito; Sakata Yasushi Sakata; Masayoshi Sarai; Daisuke Sato; Shinya Shiraishi; Yoshinobu Suwa; Kentaro Takanami; Kazuya Takehana; Junichi Taki; Nagara Tamaki; Yasuyo Taniguchi; Hiroki Teragawa; Nobuo Tomizawa; Kenichi Tsujita; Kyoko Umeji; Yasushi Wakabayashi; Shinichiro Yamada; Shinya Yamazaki; Tatsuya Yoneyama; Mohammad Rawashdeh; Daultai Batyrkhanov; Tairkhan Dautov; Khalid Makhdomi; Kevin Ombati; Faridah Alkandari; Masoud Garashi; Tchoyoson Lim Coie; Sonexay Rajvong; Artem Kalinin; Marika Kalnina; Mohamad Haidar; Renata Komiagiene; Giedre Kviecinskiene; Mindaugas Mataciunas; Donatas Vajauskas; Christian Picard; Noor Khairiah A. 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    • Contributors The study was designed by AJE, MCW, LS, YP, NB, RC, SD, PR, TCV, JV, TNBP, MD and DP. Data were provided by members of the INCAPS COVID Investigators Group. Data were curated by YP, CH, EM, BG and MR. Statistical analysis was performed by MCW and CH. MCW drafted the manuscript. All authors reviewed and edited the manuscript. AJE is the guarantor of the study.

    • Funding This study is supported by the International Atomic Energy Agency.

    • Disclaimer The views expressed in this publication are those of the author(s) and not necessarily those of the NHS, the National Institute for Health Research, or the Department of Health and Social Care.

    • Map disclaimer The inclusion of any map (including the depiction of any boundaries therein), or of any geographic or locational reference, does not imply the expression of any opinion whatsoever on the part of BMJ concerning the legal status of any country, territory, jurisdiction or area or of its authorities. Any such expression remains solely that of the relevant source and is not endorsed by BMJ. Maps are provided without any warranty of any kind, either express or implied.

    • Competing interests PM-H is a shareholder of Neumann Medical. No other authors report conflicts of interest.

    • Provenance and peer review Not commissioned; externally peer reviewed.