The 2019 Bo Lindell Laureate Lecture: On the use of interdisciplinary,stakeholder-driven,radiation protection research in support of medical uses of ionising radiation

Abstract

Medical exposures form the largest manmade contributor to total ionising radiation exposure of the UK population. In recent years, new technologies have been developed to improve treatment and prognosis of individuals treated with radiation for diseases such as cancer. However, there is evidence of public, patient, and medical professional concern that radiation protection regulations and practices, as well as understanding of potential long-term adverse health effects of radiation exposure (in the context of other health risks), have not always ‘kept pace’ with technological developments in this field. This is a truly complex, multi-disciplinary problem for the modern world.

The ‘Radiation Theme’ of the Public Health England and Newcastle University Health Protection Research Unit on ‘Chemical and Radiation Threats and Hazards’ is addressing this need, with a key focus on a genuinely interdisciplinary approach bringing together world-leading epidemiologists, radiation biologists, clinicians, statisticians, and artists. In addition, the project has a strong grounding in public, patient, and medical professional involvement in research. Similarly, the EU-CONCERT-funded LDLensRad project seeks to understand the mechanisms of action of low-dose ionising radiation in the lens of the eye, and the potential contribution to the development of cataract – in contemporary research, such projects will only be considered successful when they make use of expertise from a variety of fields and when they are able to demonstrate that the outputs are not only of benefit to society, but that society understands and welcomes the benefits. Finally, successful engagement, training, and retention of early career scientists within this field is crucial for sustainability of the research. Herein, the contribution of embedded interdisciplinary working, stakeholder involvement, and training of early career scientists to recent advancements in the field of medical (and wider) radiation protection research is discussed and considered.

1. INTRODUCTION

Medical radiation protection is a topic of current interest worldwide. As new technologies are developed, it is hugely important that radiation protection legislation and guidance keeps pace, in order to derive the benefits of the new techniques while providing adequate protection and reassurance to the individuals occupationally exposed in medical settings and their patients (Journy et al., 2016).

As the international organisation that advances, for the public benefit, the science of radiological protection through provision of recommendations and guidance on all aspects of protection against ionising radiation, the International Commission on Radiological Protection (ICRP) is at the forefront of efforts in this area, with a number of key publications focused on medical radiation protection (ICRP, 2000, 2001, 2007, 2012, 2017). The new European Union (EU) Basic Safety Standards (BSS, 2014) reduced the dose limit for the lens of the eye, for example, on the basis of epidemiological evidence reviewed by ICRP (2012) for a lower threshold than previously thought. However, the ICRP recommendations concluded with a clear statement that the radiobiological, mechanistic evidence regarding the action of low-dose ionising radiation on the lens of the eye and other tissues is still lacking (ICRP, 2012).

In terms of medical protection, a number of recent authors have looked at whether tracking patient exposures and doses might further enhance patient safety (e.g. IAEA, 2019). At first glance, the use of complete historical information on prior exposure to underpin justification and optimisation would seem an obvious tactic; however, as the very recent review of Walsh et al. (2020) pointed out, this can also lead to problems if the users of the information do not have sufficient understanding of cumulative doses, not least due to the lack of evidence for a link between individual cumulative dose and individual long-term risk.

A key theme of contemporary research is the need for genuinely interdisciplinary working. This is nothing new; indeed, Stannard (1966) considered health physics and radiation protection as two of a collection of the ‘new biology’ interdisciplinary sciences. In 1993, Galas highlighted the need for interdisciplinary research in elucidation of the mechanisms of radiation carcinogenesis (Galas, 1993). However, interdisciplinary working as standard is actually still a relatively novel approach that has not been widely adopted. In 2005, Moeller discussed the emerging interdisciplinary nature of environmental health physics in general (Moeller, 2005). By the early 2000s, following the recommendations of the High Level Expert Group on European Low Dose Risk Research (http://www.hleg.de/), the importance of research to reduce uncertainties in risk assessment of low and protracted ionising radiation exposures was of such high priority that the ‘Multidisciplinary European LOw Dose Initiative’ (MELODI) was initiated in Europe in 2010. The objective of MELODI was, and remains, integration of national and EC (Euratom) research with the key aim of promoting and supporting multi-disciplinary radiation protection research (Belli et al., 2011). Most recently, MELODI has been participating in the CONCERT European Joint Programme for the Integration of Radiation Protection Research, which seeks to contribute to sustainable integration of European and national research programmes in radiation protection (https://www.concert-h2020.eu/). Again, multi-disciplinary research is recognised as fundamental to the development of understanding to underpin effective radiation protection legislation and guidance. Such approaches have been demonstrated to lead to effective improvements in protection practice too; for example, in 2016, Moore reviewed interdisciplinary working in digital radiography protection, and concluded that interdisciplinary approaches to quality improvement, incorporating all relevant stakeholders, will lead to improvements in the associated radiation protection (Moore, 2016).

Further to this, it is now well understood that the engagement and involvement of stakeholders is a crucial part of interdisciplinary working, both in research and in policy development and implementation in the field of radiation protection and emergency preparedness (Alexander et al., 2005; Liutsko and Cardis, 2018). Genuine involvement of stakeholders, including the general public, comes with a number of challenges; however, the benefits are clear, and these include building mutual trust and understanding with all sectors of society, promoting adequate communication and reducing misinformation, and contributing to the development of robust and practical strategies for disaster recovery (e.g. Liutsko et al., 2020). However, a recent review undertaken as part of the EU CONCERT ENGAGE project identified that, while integration of industrial partners is relatively widespread, comprehensive involvement of wider sectors of society, particularly members of the public and patients, is still not standard practice in radiation protection research and development (Pölzl-Viol et al., 2018).

Finally, the training and career development of early career scientists is recognised as the foundation of an active, healthy, research community (Boice, 2017; Bradshaw et al., 2018; Ottolenghi et al., 2019a). Sustainability of research depends on maintenance of a skilled workforce, yet many areas of radiation protection research still struggle to address this need (Ottolenghi et al., 2019b).

This paper discusses how interdisciplinary working, stakeholder involvement, and training of early career scientists in a number of research projects involving the 2019 Bo Lindell Medal for the Promotion of Radiological Protection Awardee, have contributed directly to recent advancements in the field of medical (and wider) radiation protection research.

2. Interdisciplinary Working, Stakeholder Involvement, And Early Career Scientists In Medical Radiation Protection Research

2.1. NIHR HPRU Radiation Theme

The Radiation Theme of the UK National Institutes for Health Research (NIHR) Health Protection Research Unit (HPRU) on Radiation and Chemical Threats and Hazards at Newcastle University, in partnership with Public Health England (PHE), was initiated with the aim of exploring how ‘low-dose’ medical radiation exposures (chiefly procedures involving x rays) affect population health, and how modifications in the utilisation of radiation might lead to improvements in population health outcomes. In the short term, the aims were to determine the risks for medically exposed populations in the context of other health risks, to use in-vitro approaches to identify novel biomarkers of exposure, and to determine the variability in clinical response in relation to biomarkers and measures of exposure in patients undergoing radiotherapeutic procedures. In the longer term, the objectives were to provide the evidence base for safe use of low-dose medical radiation exposures, and use a multi-disciplinary approach to further advance radiation protection in the medical context.

Since the start of the project in 2015, the Radiation Theme collaborators have investigated how the use of medical x rays could affect public health at various levels, with input from a variety of disciplines including radiobiological, dosimetric, and epidemiological. Work completed includes collection and, importantly, dissemination to the scientific and wider community of evidence to demonstrate that risks associated with having medical x rays as part of certain types of investigations are very small and are likely to be significantly outweighed by the benefits of carrying out the medical procedures. For example, epidemiologists at the University of Newcastle have increased the size of the UK CT scan study cohort to over 450,000 individuals (Bernier et al., 2019), which has provided a sufficiently large population for the Radiation Theme partners to investigate how computed tomography (CT) risks might be modified by underlying health conditions (Harbron, 2016) or other confounders (e.g. transplantation status) (Harbron et al., 2018a), together with improved dose assessment (Harbron et al., 2016) and overall risk of cancers (Journy et al., 2016, 2017; Harbron et al., 2017a, 2018a) for low-dose medically exposed populations. In the area of radiobiology, key recent outputs include development and validation of cytogenetic and genetic biomarkers of radiation exposure in medically exposed populations to underpin dose assessment (Cruz-Garcia et al., 2018; Einbeck et al., 2018; Moquet et al., 2018; O’Brien et al., 2018; Tichy et al., 2018), development of a new method of premature chromosome condensation to increase the speed of biological assessment of higher doses (Sun et al., 2019, 2020), development of a new protocol for rapid gene-expression-based dose estimation (Polozov et al., 2019), and identification of further new genes suitable for biodosimetric purposes using rapid long-read DNA sequencing methods (Cruz-Garcia et al., 2020). Other major contributions include publication of peer-reviewed papers focused on the dose to the lens of the eye following CT scan exposures (Harbron et al., 2019), and the limited impact of iodinated contrast media on doses to haematopoietic stem cells (Harbron et al., 2017b, 2018b).

2.2. EU CONCERT LDLensRad Project

Human studies, for instance of the atomic bomb survivors, have led to the conclusion that the lens of the eye is more sensitive to ionising radiation exposure than previously thought (ICRP, 2012). New, substantially reduced dose limits came into force in Europe in early 2018 (BSS, 2014). However, it is still very unclear how low-dose ionising radiation might cause or be involved in the development of cataracts. This is an important current public health issue, particularly for medical radiation workers, many of whom will need to amend their working practices despite a clear lack of understanding of the effects of chronic, low-dose ionising radiation exposure of the lens of the eye.

The EU-CONCERT-funded LDLensRad project aimed to bring together experts from across Europe to answer a number of key research questions on this topic, including how does low-dose radiation cause cataracts, and how do genetic background and age influence cataract development after radiation exposure? Outcomes were anticipated to include information regarding the shape of the dose–response curve and thus the risk of radiation cataract at low doses (relevant for EU radiation workers), and thereby strengthen the evidence base for informed radiation protection.

The project results can be summarised as follows. Firstly, the partners have clearly demonstrated that both the dose and dose rate of ionising radiation are important in terms of how the lens of the eye responds to the radiation. Importantly, doses as low as a few mGy were found to cause quantifiable changes in the lens. Further, the long-term studies clearly demonstrated that genetic background, age, and sex are also important in the response and, further, these factors influence each other. Taken together, the data also advance our understanding of how ionising radiation is involved in radiation cataract formation, although unanswered questions concerning mechanisms, latency, and threshold remain. It is important to note that the project data were obtained using animal and cellular models, and human studies need to be carried out to better understand the mutual influence of these and other factors, and to understand whether the current radiation protection legislation and guidance might need to be reviewed (Ainsbury et al., 2020).

2.3. Interdisciplinary working, stakeholder involvement, and training of early career scientists in these projects

The recent results, publications, and outputs from the projects discussed in this article have involved contributions from scientists from a variety of backgrounds. While some publications concern a single research topic, in most cases, the research would not even have been conceived were it not for interdisciplinary collaboration, for example between epidemiologists, dosimetrists, and lens biology specialists for the work on doses to the lens of the eye under the Radiation Theme, and between dosimetry specialists, radiation biologists, and pathologists for the findings of the LDLensRad project. There are further examples too numerous to mention from both projects and, indeed, examples of the projects working together too – the key point being that interdisciplinary working has been fully imbedded in both of these projects.

As outlined in the sections above, the research findings have resulted in many peer-reviewed publications, and the work has also been presented at numerous international scientific conferences. Here, the impact of such interdisciplinary working is also clear – not only in the volume of publications addressing a large number of different questions associated with use of low-dose ionising radiation in medical contexts, but also where medical radiation protection research has direct input from medical professionals; as discussed below, the outputs include suggestions on how medical practice can be altered to improve protection and limit doses.

Furthermore, members of the public have been actively involved in every stage of the projects – chiefly through membership of the Radiation Theme management board, attendance of biannual project-wide meetings for HPRU, and attendance of focused events for the LDLensRad project. Indeed, several of the publications contain ideas which originated during discussions with the ‘lay’ members of the team – the work on dose to the lens of the eye is an example of this. Project members from all disciplines have also been involved in a number of stakeholder dissemination activities, including workshops, to explain and elicit public response to the research. At a series of ‘Public and Patient Involvement’ workshops over the course of HPRU and LDLensRad projects, scientific stakeholders and members of the public have had the opportunity to talk directly to researchers about their work, to ask questions and explain their thoughts on the use of ionising radiation in society, and how the research contributes to radiation protection and safety. One such event – the PHE workshop on medical professional, public, and patient involvement in research into radiation cataract and radiation protection of the lens – took place in May 2018, with the following aims: to give the early career researchers involved the opportunity to outline current scientific understanding and need for scientific research on radiation cataracts to a non-research audience; to present the aims of the LDLensRad project and associated HPRU work; to highlight how the lens research programme fits in with PHE’s wider health protection functions, and to answer any questions arising and collate comments and suggestions for the researchers from the attendees. The attendees included a cross-section of medical professionals, chiefly from hospital radiology departments, patients recently exposed to medical radiation, and interested members of the public. Presentations on the projects from the predominantly early career researchers, as a key element of their training, were followed by a detailed discussion with the attendees of their impressions of the research and how it has been communicated, aided by the following questions:

Question 1. What are your overall impressions of the project as a whole?

Question 2. Can you see how the project contributes to PHE’s core aim of protecting health and wellbeing?

Question 3. Have we managed to convince you that this research is important and necessary, and a good use of public money?

Question 4. Is there anything you think we could/should do differently?

Question 5. What do you think are the best ways to involve key stakeholders (you!) in the project going forward?

Question 6. How can we best disseminate our results to the public and medical professionals?

Regarding the projects themselves, the feedback received was excellent – all participants who answered these questions agreed that the project is legitimate and worthwhile in the face of new information on risk to the lens of the eye to inform setting dose limits, that the projects are a good use of taxpayers’ money and a great example of multi-disciplinary working, and that stakeholder engagement of the type encouraged by the workshop is important too. Use of radiation in medical practice is increasing, and hospitals already have medical staff reaching the new dose limits so operational changes will be needed. Further, the culture in some hospitals/departments is still quite different to nuclear facilities; for example, where failing to wear personal protective equipment would mean immediate disciplinary action. Further dissemination and direct training will be hugely important going forward. Medical colleagues also welcomed the discussions around potential future studies, some of which could involve them or their departments, for instance, to focus on how practice can be modified to avoid lens exposures while not diminishing image quality or missing pathologies, whether this depends solely on technical capability or training. In a key example of direct impact for this type of activity, the medical professionals present left saying that they would check/amend practice in their own hospitals to ensure that doses to the lens of the eye are limited.

In terms of the format of the event, the participants thanked the speakers for giving clear presentations, making their research easy to understand. The attendees felt that they had received more information than expected, which had exceeded their expectations; that the mixed audience had worked well as it further facilitated genuine discussion; and this was a very good way to garner genuine stakeholder involvement and feedback. Many attendees praised the relaxed atmosphere fostered from the start, which meant that all participants felt comfortable contributing their thoughts and ideas despite the wide range of backgrounds and fields of expertise. The lay representatives also mentioned that they felt equally valued and trusted, and that while they had not all appreciated the risk to the lens of the eye (indeed, some were sceptical beforehand!), they could now see why it was important to consider this as well as more commonly understood risks such as cancer, and were reassured that such research is taking place.

The fact that the LDLensRad and HPRU projects were presented in the context of PHE’s wider programme of radiation and health protection was also appreciated, as it presented a united front, and it was clear to all participants who answered Question 2 that the projects fit PHE’s core aims around health and wellbeing. However, some external participants were surprised when PHE representatives informally reported that this type of interdepartmental working was quite unusual, and suggested that such collaboration should take place more often; for instance, LDLensRad researchers could be more closely involved in development of practical guidance for medics to ensure a ‘joined-up’ PHE-wide approach.

In terms of how the projects or such events might be improved, it was suggested that the initial presentation of the LDLensRad project could have been more succinct, giving more detail (e.g. on plans and timescale), and some participants felt that more details on the ‘bigger picture’ of the project itself would have been useful, rather than just presenting some distinct aspects. The pre-meeting telephone briefing for lay attendees had been appreciated, but other attendees also felt that they would have benefited from this. It was also suggested that an additional presentation on how medical professionals use radiation, together with an explanation of the risk/benefit balance, could have been included to ensure that was clear to all the lay attendees. Wider dissemination of the strategy at an early stage was also encouraged. For future project involvement and dissemination events, it was suggested that such events should take place at an earlier stage – at the beginning or even before the research starts – to further facilitate genuine stakeholder input. The attendees also suggested some potential additional engagement activities, including joining wider events such as the Harwell Campus open day or New Scientist Live.

Going forward, participants agreed that another such meeting closer to the end of the project, when more results are available, also involving the European partners, would be useful. In addition, telephone discussions with the stakeholder group and for wider dissemination – leaflets, posters (e.g. in radiology department waiting rooms and staff rooms), contribution to relevant guidance, publication of reports or other project details on the PHE website, production of a newsletter, presentations at relevant conferences (e.g. PHE conference) and to relevant professional organisations (e.g. Society and College of Radiographers, British Institute of Radiology, Institute of Physics and Engineering in Medicine), public announcements and e-mails to interested parties, writing articles for other websites or magazines (e.g. Synergy News – magazine of the Society of Radiographers), making use of the stakeholder group established following this workshop to disseminate information amongst colleagues, and use of modern technologies including podcasts, blogs, and social media – were considered to be useful. The participants were also asked whether they would be willing to keep in contact in order to contribute to additional events. All participants answered positively and have therefore been added to the project stakeholder distribution list.

In conclusion, this event clearly demonstrated that the principles of good practice from experience in other projects developed in partnership with social scientists and radiation protection scientists (Liutsko et al., 2020), particularly early face-to-face meeting of project partners and stakeholders, and the importance of clear and concise messages, facilitated successful stakeholder contributions to these projects. Further, the early involvement of stakeholders enabled suggestions on engagement and dissemination within the projects to be incorporated into the project policies on this as they progressed. As a result of this activity and similar activities throughout the projects, early career scientists gained key experience in stakeholder involvement as a hugely important aspect of modern research, and public and industrial stakeholder support for the work and the outputs is also clearly documented. Key lessons learnt as a result of this activity include keeping in regular contact with all stakeholders willing to participate – they are a fantastic resource. In future activities, the recommendation of Liutsko (2020) around use of specific training courses for stakeholders who will use the project outputs will certainly also need to be considered.

3. DISCUSSION AND CONCLUSIONS

As noted in Section 1, the benefits of multi-disciplinary working, stakeholder engagement and involvement, and education and training of early career scientists have been addressed by many authors and are absolutely clear (Ottolenghi et al., 2019b; Liutsko et al., 2020). Indeed, in recent years, most, if not all, grant calls now ask for clear details of at least components of these to be addressed within the grant application. As such, it is within the interests of all members of our research community to fully engage with engagement.

Within the EU CONCERT project, a huge amount of work has been done to promote interdisciplinary working, stakeholder engagement and involvement, and education and training. As a result of this, researchers in the field of radiation protection research are now in an excellent position – many models and tools are available to support these activities. Further, it is the responsibility of all active scientists, project managers, and funding recipients to support sustainability within the fields of radiation protection research by recruiting, training, and supporting early career scientists. These key components are required for successful research projects which are genuinely able to contribute to scientific and policy developments in the field of radiation protection.

The projects discussed in this article give examples of how the use of interdisciplinary relationships, stakeholder involvement, and early career scientists can facilitate provision of clear evidence regarding the long-term safe use of ionising radiation in medicine. Such work underpins advice for medical staff regarding provision of informed consent, and reassurance for patients that procedures are safe and justified. Further, the direct impact of such activities is also clear – the lens dosimetry work, for example, has led to document changes in hospital practice around shielding of the lens of the eye during head and neck procedures.

However, there are still improvements to be made – for example, although the HPRU Research Theme had members of the public sitting on the project management board, the LDLensRad project rather relied on specific events focused chiefly on stakeholder dissemination and elucidation of comments/ideas, which is not necessarily the best way to facilitate regular genuine stakeholder involvement. For both projects, members of the public have been identified as the key stakeholders, and while the LDLensRad project has also involved industrial partners, wider stakeholders have not been as actively involved in the Radiation Theme as they could have been.

Ultimately, as with all projects, interdisciplinary working, the involvement and active training of early career scientists in both projects, and – to a certain extent – stakeholder involvement have relied on the need for these areas being specified in the grant calls, and also on them being facilitated by the funding models. It is very important to note that, as described here, mandating of these activities does not preclude them being of real benefit. As always, further work needs to be done to ensure that all research projects in this area recognise the importance of these activities in terms of generation of innovative answers to the open research questions, promoting communication on this important topic within society to build mutual trust and understanding and for long-term sustainability, and thus follow such models going forward. Furthermore, sustainability of research does not rely solely on funding, training, and retention of early career scientists; going forward, this also implies the additional consideration of environmental aspects of research – including (but certainly not limited to) the wider environmental and non-human implications of the use of ionising radiation in society and the research methods employed in this field (e.g. Vandenhove et al., 2018), and the use of video and other conferencing facilities to replace travel to limit the carbon footprint of research. Only by considering all of these aspects will radiation protection research be genuinely integrated into society, and be seen to be socially responsible and well oriented to address the needs of society.