key: cord-1011489-jg2h11yd
authors: Vagal, Achala; Reeder, Scott B.; Sodickson, Daniel K.; Goh, Vicky; Bhujwalla, Zaver M.; Krupinski, Elizabeth A.
title: The Impact of the COVID-19 Pandemic on the Radiology Research Enterprise: Radiology Scientific Expert Panel
date: 2020-04-15
journal: Radiology
DOI: 10.1148/radiol.2020201393
sha: 74f9ff60a50f989fe55313d4a1e8b129daf44927
doc_id: 1011489
cord_uid: jg2h11yd

The current COVID-19 crisis continues to grow and has resulted in marked changes to clinical operations. In parallel with clinical preparedness, universities have shut down the majority of scientific research activities. Radiology researchers are currently grappling with these challenges that will continue to affect current and future imaging research. The purpose of this article is to describe the collective experiences of a diverse international group of academic radiology research programs in managing their response to the COVID-19 pandemic. The acute response at six distinct institutions will first be described, exploring common themes, challenges, priorities, and practices. This will be followed by reflections about the future of radiology research in the wake of the COVID-19 pandemic.

The COVID-19 pandemic has led to major changes in the clinical operations of radiology departments world-wide. 1 In parallel with clinical preparedness activities, academic medical centers and universities have rushed to shut down scientific research activities to maximize social distancing and minimize the spread of infection to research staff and others with whom they might have contact. The definition of "essential" research-related activities narrowed rather quickly, until very few research personnel are now on site in radiology departments. The rapid suspension of radiology research operations has created numerous challenges with both short-term and longterm implications.

The purpose of this article is to describe the collective experiences of a diverse international group of academic radiology research programs in managing their response to the COVID-19 pandemic. In addition, the authors assess the future of Radiology research in the wake of the COVID-19 pandemic.

Research at the University of Cincinnati (UC) Department of Radiology is centered around four institutes, devoted to neuroscience, cancer, cardiovascular disease, and diabetes and obesity, respectively and is predominantly concentrated on clinical trials. UC also hosts the national coordinating center for the NIH/NINDS Stroke NET, supporting a robust infrastructure of approximately 400 clinical performance sites, and managing large Phase II and Phase III stroke trials.

As the pandemic gained momentum in our area, we prepared for an imminent and sustained reduction in on-campus research. A day after the state of Ohio issued a 'stay at home' order, we transitioned to a 'level 1' research status, wherein only approved critical research activities on campus were allowed. These activities were predominantly limited either to a) COVID-19-related research or b) medical research that, if discontinued, would endanger the I N P R E S S lives of participating human subjects. We discontinued all human subjects research studies involving in-person interactions except those programs with explicit institutional and Internal Review Board (IRB) approval to continue ( Table 1) .

Our top priority has been the safety of our research team members and the participants in our research studies. Our secondary priority is to preserve the scientific integrity of our research protocols. We put in place guidelines for study enrollment including screening for COVID-19 symptoms, particularly for studies involving direct contact with human subjects. To achieve social distancing, we transitioned all research staff to work from home, provided contact information for all research team members, and updated the research group with clear communications. We gave research team members remote access to lab computers, files, data and software systems and maintained Health Insurance Portability and Accountability Act (HIPAA) compliance and data control assurances.

Continuing productivity during the discontinuation of research programs: We expect significant disruptions to research operations, facility access and staff availability for at least the next three months. Therefore, we have developed a continuity-of-operations plan for our research program. This includes setting up imaging infrastructures for upcoming new trials such as building imaging charters, central reading manuals and case report forms. We instructed research staff to devote time to productive off-site alternative research activities, such as writing grant proposals and manuscripts, reviewing articles, compiling data, conducting data analysis, and synthesizing literature. We are encouraging staff to learn new skill sets, start online writing groups and maintain weekly progress trackers. Some research coordinators have been redeployed to support clinical needs (e.g., rescheduling of non-urgent imaging). We have also joined in COVID-related research activities and working with colleagues in medicine and engineering to 3D print components for face shields, N95 masks, nasal-based PCR tests, ventilator splitting apparatus, and touchless door handle openers.

In these times of uncertainty, it is particularly critical to attend to physical and mental wellbeing (Table 2) . We continually circulate wellness resources for research staff and promote morale-building activities such as virtual water-cooler conversations, virtual fitness challenges and mindful movement sessions. Our ongoing goal has been to maintain both individual and team morale in the midst of what promises to be an extended crisis.

The University of Wisconsin (UW) Department of Radiology has centralized many of its research operations at a single large facility encompassing basic and translation imaging research in MRI, CT, PET and radiopharmaceuticals and ultrasound. Over 350 imaging researchers, including faculty, staff scientists, post-doctoral fellows, graduate students, research staff, and research administrative staff are located in our primary imaging research center, which is attached directly to the main UW hospital and clinics. In our radiology research operations, we instituted a rapid response to the COVI9-19 pandemic:

Health and safety of employees and research subjects: The safety and welfare of employees, trainees and research subjects has been our highest priority. We initiated an urgent effort to halt non-essential on-campus research activities. All employees and trainees not engaged in essential research activities were instructed to go home, bringing necessary materials and equipment such as laptop computers to enable them to work from home for an extended period.

Restricted access and exceptions for essential research: 24/7 key card access was initiated to restrict access our primary imaging research center. All non-essential on-campus research was addressing new issues as they arose. Continued efforts are ongoing to provide remote computer access for researchers, while ensuring that appropriate HIPAA protections are maintained for human subjects research. Even with remote access to computer systems, the lack of access to imaging equipment has, of course, presented a major challenge for technical development.

We have paid special attention to the wellness of all of our staff and students, via frequent one-on-one communications, virtual video-based social gatherings, and online yoga sessions (Table 3) . Information on accessing campus resources provided by employee health services (including mental health services) has been disseminated to all staff and trainees. We are developing policies that will accommodate delays in graduate degree programs for radiology researchers. UW has initiated a tenure clock extension for junior faculty, and strategies for bridge funding are being formulated within radiology and on campus. Protecting our research teams: As infection rates kept rising, our key priority was to get our people home. We shared centralized telework resources (VPN-virtual private network, videoconferencing access, etc), and encouraged all research staff to prepare to work from home for an extended period, with computers and other equipment taken as needed from the office or purchased anew. Within a week, our research offices were empty, and entry was off limits to anyone without explicit permission from research leadership.

Promoting wellness in during the COVID-19 pandemic. This forced diaspora of our research team placed a new premium on communication. Our research leadership team, which met frequently online, began sending out daily updates. We established a weekly online meeting for all research staff, as a clearinghouse for questions and ideas. With coronavirus-related I N P R E S S information flowing in from all sides, these communications were targeted at the interests and concerns of researchers. This included the current policies for nonessential staff, the latest notices from the National Institutes of Health (NIH), reimbursement of meeting cancellation expenses, tenure clock extensions, and resources for mental health and wellness. Our researchers are also organizing virtual coffee hours, social networking channels, targeted research group meetings, and other modes of connecting.

Contribution of radiology research to fighting the pandemic: Our research teams have convened around helping to mitigate the COVID-19 crisis. Our 3D printers are being used to print face shields for emergency clinical use. Our department's collaboration with Facebook has been redirected to develop machine learning models for COVID-19 diagnosis, as well as prediction of disease course and severity, based on chest X-ray and other clinical data. We are participating in COVID-19 data-sharing consortia with other medical centers and imaging societies. Our researchers are developing projects in response to COVID-19-related NIH requests for proposals.

Our research staff is also preparing educational lecture series on imaging research for trainees and clinical staff. While our research teams actively pursue ways to contribute to defeating the pandemic, we are also working with clinical teams to increase imaging efficiency, in order to meet increased demand when backlogged elective imaging studies resume at the conclusion of the current pandemic crisis. to be essential to the health and/or well-being of the subject. Some essential trials, plus certain clinical scans, required that personnel associated with cyclotron and radiochemistry operation come into work periodically (following all standard safety and social distancing precautions).

Ongoing animal trials are allowed to continue to the point where they can feasibly be put on hold.

Those associated with newly developed animal trials are allowed to commence with proper approvals in place. Research faculty have contributed any extra PPE (e.g., masks or goggles) or related resources to our hospital facilities.

While physical wellness is foremost on everyone's mind during the current crisis, we have also sought to support the mental and emotional wellness of our research staff. We have encouraged our teams to keep things as 'normal' as possible, with regularly-scheduled lab calls (preferably including video), regular work hours, and other simple expedients, such as changing clothes for work hours, scheduling physical activity (especially if that activity can involve family), and virtual coffee breaks. We have encouraged supervisors to keep information flowing, and to make themselves available to their teams as much as possible.

The Department of Radiology at King's College London is affiliated with the School of Biomedical 

We anticipate important negative sequelae on radiology research programs after the conclusion of the COVID-19 pandemic (Table 4 ). If not specifically addressed, the current disruption of imaging research will have adverse ramifications for productivity, funding, and scientific progress in the future. A shutdown of 3-4 months will likely result in as much as 1-2 years of lost scientific productivity. For example, when clinical trials resume, investigators will have to deal with missed visits, and protocol deviations (although a significant amount of groundwork can be carried out now to jumpstart activities once re-initiated). Further, we anticipate challenges with re-engaging existing subjects and recruitment of new subjects, including possible reticence of subjects to visit medical environments. Missing data will greatly impact trial results and interpretation, possibly stopping some trials altogether. Another example of disruption is the current suspension of the national IRB process in the UK, which will inevitably result in significant backlog and delays after I N P R E S S submission reopens. Many US IRBs are only reviewing COVID-related studies, creating potential for future delays as well.

Radiology research funding will also be a central challenge. Departmental and institutional budgets will undoubtedly be constrained in the wake of the pandemic. This may lead to significant retrenching of research expenditures in radiology departments. Clinical revenue typically offsets the costs of imaging research funded through extramural support. Radiology departments are currently experiencing an abrupt drop in clinical revenues due to sharp declines in non-urgent imaging volume. As a result, departments may be forced to make difficult decisions regarding research support in subsequent budget cycles. Imaging research could potentially be devalued during the post-COVID-19 period, when departments are focused on recovery of clinical operations and revenues. This effect may persist for many years and there is a real risk that some imaging research programs may never fully recover.

In addition, research equipment purchases will be delayed or cancelled with shrinkage of capital budgets. National funding organizations, such as the NIH in the US or the NIHR in the UK, are offering flexibility in the conduct of projects affected by the crisis, and there may be benefit in the short term from COVID-related stimulus packages. However, the emerging worldwide economic downturn is certain to impact long term national research budgets. The impact on industry partners is also likely to be significant, not just those supporting clinical trials, but those with whom institutions have master research agreements that support research, equipment purchases and many other related activities. This may be especially impactful for smaller companies and those developed by our more entrepreneurial faculty.

Another challenge will be the ability to publish research and submit grants without access to laboratories and imaging equipment, which are necessary to generate essential preliminary data. In light of our current "work at home" paradigm, we call on journals and funding organizations I N P R E S S to accommodate publication of manuscripts and review of grant submissions without the level of laboratory-based data required under normal circumstances.

The disposition of research hiring is also a matter of concern. Given anticipated funding constraints, uncertainties about future travel, and potential restrictions in immigration policies, many institutions are already imposing hiring freezes. Staff retention is also precarious, particularly those funded by clinical or departmental funds. Loss of highly trained academic research personnel is anticipated, either due to lack of work with accompanying furloughs or layoffs, or through loss to industry. Recovery from the loss of highly experienced personnel may take decades, if ever, and will place considerable additional pressure on our remaining research work force. Similarly, imaging service centers and cores that rely on revenue to maintain expert staff are also at risk. These service centers will require varying degrees of financial assistance to recover revenue and to continue to function once the demand for research services begins to ramp up. Junior faculty, fellows and students may struggle to meet deadlines for promotion or graduation, which may in turn negatively impact future job prospects.

Meanwhile, interruption in the exchange of scientific ideas due to cancellation or postponement of annual meetings of major scientific societies will significantly impact global scientific progress. Imaging societies that host meetings and maintain other key connective activities are under existential pressure from current and future lost revenues. Larger and financially solvent societies will simply delay or cancel their annual meeting for ~1 year, while smaller or less financially viable societies may be impacted more severely. This will be compounded by reduced professional development expenditures provided by radiology departments to their personnel, who will ultimately attend fewer society meetings.

What can the radiology and imaging research communities do to ensure that we not only survive but also manage to thrive under such uncertain conditions? We believe that future of radiology research should be reconsidered. Even as the artificial intelligence (AI) tsunami has I N P R E S S rolled through Radiology, we have been slow as a field to create platforms for broad-based image and data sharing. The COVID-19 pandemic has highlighted, with shocking urgency, the importance of data sharing and rapid mobilization of disseminated research teams. RSNA recently announced the COVID-19 Imaging Data Repository initiative which will allow image hosting, annotation and analysis framework for researchers. 2 Additional disease specific imaging biobanks linked to other biorepositories would need to be disseminated widely. Lobbying for additional funding for imaging and health informatics, has never been more important.

Nursing staff, emergency physicians, and critical care specialists are clearly on the front lines of our current battle against the coronavirus. Even though radiologists, particularly in nonpulmonary and non-emergency subspecialties, may not be in the public eye right now, the tools that radiology offers continue to offer key insights, and imaging research after COVID-19 will be more important than ever for human health. Dedicated advocacy efforts through organizations such as American College of Radiology (ACR) and Academy for Radiology & Biomedical Imaging

Research will be essential to inform the public and policy makers on the importance of continuing innovative imaging research. It is up to us to continue to innovate and create new opportunities to advance imaging research.

Common challenges and strategies (Table 1) , mechanisms for maintaining morale and wellness in research personnel (Table 2) . special groups in research team to consider (Table 3 ) are a priority for radiology research programs. As our priorities shift from emergency response to the eventual resumption of imaging research, we will have to face numerous challenges. We will be called upon to rethink some of our accustomed processes. We will have to engage with leaders, funding agencies and the general public as we navigate the post-coronavirus world. The actions we take now, and the plans we put in place, have the potential to change the shape of imaging research for many years to come. If not specifically addressed, disruption of imaging research will have adverse ramifications for radiology and imaging sciences:

� A 3-4 month pandemic shutdown is estimated to result in up to 1-2 years of lost research productivity � Potential for reduced radiology research funding due to economic impacts of the pandemic on universities � Potential for delay in equipment purchases with reduced capital budgets, otherwise necessary for state-of-the-art research programs in radiology � Potential for reduced innovation and publishing in imaging research due to lack of access to imaging equipment and research labs 

Radiology Department Preparedness for COVID-19: Radiology Scientific Expert Panel