key: cord-0842314-orx1pm03
authors: Williams, Michelle Claire; Shaw, Leslee; Hirschfeld, Cole B; Maurovich-Horvat, Pal; Nørgaard, Bjarne L; Pontone, Gianluca; Jimenez-Heffernan, Amelia; Sinitsyn, Valentin; Sergienko, Vladimir; Ansheles, Alexey; Bax, Jeroen J; Buechel, Ronny; Milan, Elisa; Slart, Riemer H J A; Nicol, Edward; Bucciarelli-Ducci, Chiara; Pynda, Yaroslav; Better, Nathan; Cerci, Rodrigo; Dorbala, Sharmila; Raggi, Paolo; Villines, Todd C; Vitola, Joao; Malkovskiy, Eli; Goebel, Benjamin; Cohen, Yosef; Randazzo, Michael; Pascual, Thomas N B; Dondi, Maurizio; Paez, Diana; Einstein, Andrew J
title: Impact of COVID-19 on the imaging diagnosis of cardiac disease in Europe
date: 2021-08-05
journal: Open Heart
DOI: 10.1136/openhrt-2021-001681
sha: 9209a5a4db9c66a2d36088f028786abc84b7687d
doc_id: 842314
cord_uid: orx1pm03

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.

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 Williams MC, et al. Open Heart 2021; 8:e001681 . doi:10.1136/openhrt-2021-001681 the centre of the diagnosis and management of coronary artery disease. However, during the COVID-19 pandemic, both guidelines [1] [2] [3] [4] [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] [8] [9] and an increase in out-of-hospital cardiac arrests 10 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.

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.

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.

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 Health care delivery, economics and global health care model. Population, GDP and COVID-19 deaths were log transformed for analysis.

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.

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). 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).

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 nonstress CMR were highest in Southern and Northern Europe (table 2) . 

3% (3) 13% (5) 3% (2) 5% (13) 25% (148) Teaching facility 74% Health care delivery, economics and global health care

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).

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).

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) .

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 onethird 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] [19] [20] [21] During the COVID-19 pandemic, several studies have reported an increase in out-of-hospital cardiac arrests 10 22 and excess cardiovascular mortality. 11 In March 2020, there was a 48% reduction in admissions with acute myocardial infarction to Italian coronary care units 23 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 syndromes 7-9 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 implantation 26 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 Health care delivery, economics and global health care 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 USA 30 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.

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

Rabie Benlabgaa; Salah Bouyoucef; Abdelkader Medjahedi

Roxana Campisi; Alejandro Canderoli; Silvia Carames; Patrícia Carrascosa; Ricardo Castro

Miguel Angel Guzzo; Victor Hasbani; Melina Huerin; Victor Jäger

Marcos Montecinos; Eduardo Noguera

Marcela Redruello; Marina Rodríguez

Girish Dwivedi; Barry Elison

Anand Gaikwad; Ashok Gangasandra Basavaraj

Victar Hsieh

Filip Homans

Agnès Pasquet

Simone Brandão; Diego Bromfman Pianta

Marcelo Hadlich; Vinícius Kameoka

Tiago Magalhães; Fábio Martins Silva

Vania Naue

Maria Eduarda Menezes de Siqueira; Cristiano Siqueira

Guilherme Urpia Monte

Estevan Vieira Cabeda; Felipe Villela Pedras

Youdaline Theng; Gad Abikhzer

Stephan Probst; Idan Roifman

Ulises González; Ana Baric; Tonci Batinic

Mladen Jukic; Petar Medakovic; Viktor Persic

Rayner Menéndez; Amalia Peix; Luis Rochela; Christoforos Panagidis

Islam Shawky Abdel Aziz; Mahasen Abougabal

Martti Larikka; Valtteri Uusitalo

Vincent Habouzit; Fabien Hyafil

Franck Proffit

Aikaterini Archontaki

Christina Fragkaki; Panagiotis Georgoulias; Sophia Koukouraki

Evangelos Repasos

Balint Szilveszter; Edit Várady

Jinendra Kumar Bhagat; Rishi Bhargava; Vivek Bhat

Prof Dr Girijanandan Mahapatra

Habusari Hapkido; Basuki Hidayat; Aulia Huda

Alex Frenkel; Galit Knafo

Maya Mor; Noam Muskal; Sara Ranser; Aryeh Shalev

Armando Ugo Cavallo; Giorgio Cavenaghi

Laura Evangelista; Riccardo Faletti; Evelina Faragasso; Mohsen Farsad; Paola Ferro; Luigia Florimonte; Viviana Frantellizzi; Fabio Massimo Fringuelli

Hiroshi Asano; Chimura Misato Chimura; Shinichiro Fujimoto; Koichiro Fujisue; Tomohisa Fukunaga; Yoshimitsu Fukushima; Kae Fukuyama; Jun Hashimoto; Yasutaka Ichikawa

Masamichi Imai; Anri Inaki; Hayato Ishimura; Satoshi Isobe

Takashi Kudo; Shinichiro Kumita; Hirotaka Maruno

Masao Moroi; Shigeki Nagamachi; Kenichi Nakajima; Tomoaki Nakata; Ryo Nakazato; Mamoru Nanasato

Yoshinobu Suwa; Kentaro Takanami; Kazuya Takehana; Junichi Taki; Nagara Tamaki; Yasuyo Taniguchi; Hiroki Teragawa; Nobuo Tomizawa

Shinya Yamazaki; Tatsuya Yoneyama; Mohammad Rawashdeh; Daultai Batyrkhanov

Sonexay Rajvong; Artem Kalinin; Marika Kalnina; Mohamad Haidar; Renata Komiagiene; Giedre Kviecinskiene; Mindaugas Mataciunas; Donatas Vajauskas; Christian Picard; Noor Khairiah A. Karim; Luise Reichmuth

Ambedhkar Shantaram Naojee

Andor Glaudemans; Jesse Habets; Klaas Pieter Koopmans; Jeroen Manders

Riemer Slart; Paul Thimister; Erik-Jan Van Asperen; Niels Veltman; Derk Verschure

Andrew To; Niels Van Pelt; Calum Young

Djibrillou Moussa Issoufou; Tolulope Ayodele; Chibuzo Madu

Signe Helene Forsdahl; Jenni-Mari Hildre Dimmen; Arve Jørgensen; Isabel Krohn

Zabah Jawa; Naima Tag; Muhammad Shehzad Afzal

Muhammad Numair Younis; Musab Riaz; Mohammad Saadullah

José Ortellado; Afroza Akhter; Dianbo Cao

Liming Xia; Jiangxi Xiao

Christian Michael Pawhay; Alvin Quinon; Jeanelle Margareth Tang

Ghulam Syed; Samer Arnous

Kyoung Sook Won; Venjamin Majstorov

Claudiu Adrian Stan; Alexey Ansheles; Olga Dariy; Olga Drozdova

Daria Ryzhkova; Guzaliya Saifullina

Margarita Vakhromeeva; Nailya Valiullina

Mirvat Alasnag

Andrej Vondrak; Shereen Bejai

Moshe Modiselle; Stuart More

Maria Pedrera Canal

Damayanthi Nanayakkara; Chandraguptha Udugama

Khiewvan; Teerapon Premprabha

Zerida Muyinda; Yaroslav Kmetyuk; Pavlo Korol; Olena Mykhalchenko; Volodymyr Pliatsek

Alexia Farrugia; Deepa Gopalan

Prasad Guntur Ramkumar; Mark Hamilton; Mark Harbinson

Ntouskou Marousa; Jon Martin; Elisa Mcalindon

Peter Strouhal; Deepak Subedi

Katharine Tweed

Suhny Abbara; Taimur Abbasi

Andressa Borges; Kelley Branch; Paco Bravo; Jessica Brothers

Candace Candela; Elizabeth Capasso

Saurav Chatterjee

Nimish Dhruva; Neil Doherty

Ami Iskandrian

Zorana Mrsic; Venkatesh Murthy

Jagat Narula; Katarina Nelson

Pravin Patil

Amit Pursnani; Mark Rabbat

guidance for the diagnosis and management of CV disease during the COVID-19 pandemic

Society of cardiovascular computed tomography guidance for use of cardiac computed tomography amidst the COVID-19 pandemic endorsed by the American College of cardiology

COVID-19 pandemic and cardiac imaging: EACVI recommendations on precautions, indications, prioritization, and protection for patients and healthcare personnel

Society for cardiovascular magnetic resonance (SCMR) guidance for the practice of cardiovascular magnetic resonance during the COVID-19 pandemic

Guidance and best practices for reestablishment of non-emergent care in nuclear cardiology laboratories during the coronavirus disease 2019 (COVID-19) pandemic: An information statement from ASNC, IAEA, and SNMMI : Endorsed by the Infectious Diseases Society of America

International impact of COVID-19 on the diagnosis of heart disease

COVID-19 pandemic and admission rates for and management of acute coronary syndromes in England

Reduced rate of hospital admissions for ACS during Covid-19 outbreak in northern Italy

Hospital admissions with acute coronary syndromes during the COVID-19 pandemic in German cardiac care units

Characteristics associated with out-of-hospital cardiac arrests and resuscitations during the novel coronavirus disease

Place and causes of acute cardiovascular mortality during the COVID-19 pandemic

COVID-19 and cardiovascular disease: from basic mechanisms to clinical perspectives

Multimodality imaging in evaluation of cardiovascular complications in patients with COVID-19: JACC scientific expert panel

World health organisation coronavirus disease (COVID-19) dashboard

World bank country and lending groups

Standard country or area codes for statistical use M49

Impact of cardiovascular disease and cardiac injury on in-hospital mortality in patients with COVID-19: a systematic review and meta-analysis

Factors associated with COVID-19-related death using OpenSAFELY

Factors associated with hospital admission and critical illness among 5279 people with coronavirus disease 2019 in New York City: prospective cohort study

The effect of frailty on survival in patients with COVID-19 (COPE): a multicentre, European, observational cohort study

COVID-19 kills at home: the close relationship between the epidemic and the increase of out-ofhospital cardiac arrests

Reduction of hospitalizations for myocardial infarction in Italy in the COVID-19 era

Fewer hospitalizations for acute cardiovascular conditions during the COVID-19 pandemic

The Covid-19 pandemic and the incidence of acute myocardial infarction

Transcatheter management of severe aortic stenosis during the COVID-19 pandemic

The impact of COVID-19 on the provision of cardiac surgical services

Society for cardiovascular magnetic resonance (SCMR) guidance for reactivation of cardiovascular magnetic resonance practice after peak phase of the COVID-19 pandemic

ASE statement on the reintroduction of echocardiographic services during the COVID-19 pandemic

Trends in emergency department visits and hospital admissions in health care systems in 5 states in the first months of the COVID-19 pandemic in the US

The impact of the COVID-19 pandemic on cancer deaths due to delays in diagnosis in England, UK: a national, population-based, modelling study

Acknowledgements 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 Provenance and peer review Not commissioned; externally peer reviewed.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.Open access 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/.

Michelle Claire Williams http:// orcid. org/ 0000-0003-3556-2428 Pal Maurovich-Horvat http:// orcid. org/ 0000-0003-0885-736X Chiara Bucciarelli-Ducci http:// orcid. org/ 0000-0002-2515-0852 Eli Malkovskiy http:// orcid. org/ 0000-0002-9027-7497

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.

Patient consent for publication Not required.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.