A framework for the promotion of ethical benefit sharing in health research

Introduction

Ethical management of the data and biospecimen ecosystem for health research is underpinned by a fundamental principle of balancing risks and benefits in the pursuit of respectful, equitable and meaningful research to benefit humanity (reviewed in1). While health research directly contributes to achieving the United Nations’ Sustainable Development Goal (SDG) 3, Good Health and Well-being, there is scope for the research ecosystem to provide many more benefits that can contribute to many more SDGs including reducing inequalities, contributing to socioeconomic goals and supporting sound policy-making institutions and partnerships. In figure 1, we provide examples of SDGs to which health research could contribute, such as capacity development to improve stakeholder partnerships and support institutions (SDGs 16, 17), optimising efficient and responsible use of resources for healthcare (SDGs 11, 12), stimulating economic activity through development of the health and biotech sector (SDGs 8, 9) and ensuring a healthy, employed workforce with reduced risk of poverty and hunger (SDGs 1,2, 3, 10). Health research stakeholders can also actively choose to reduce inequality and promote gender equality during their activities (SDGs 5, 10). For every health research study undertaken, in order to uphold practices that are equitable and just it is therefore important to interrogate who will take which risks, what are the benefits and to whom will those benefits accrue. Here, we discuss benefit sharing in terms of the actions taken towards ensuring that various benefits of research are shared with a wide range of stakeholders in a way that is equitable and just.

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Discourse about ensuring the fair distribution of research benefits has been ongoing for decades, emerging initially from clinical research involving human participants and subsequently extending to health genomics research.2–5 For non-human biospecimens, in relation to bioprospecting, the Nagoya Protocol aims to inculcate benefit sharing alongside material transfer agreements, but human biological resources and digital sequence information are not currently included.6–8 In 2016, the Council for International Organizations of Medical Sciences updated their research ethics guidelines to discuss benefit sharing for medical research and to advocate for negotiated benefit sharing agreements, but failed to explore the impact of inequity on the negotiating position of stakeholders in the global South.9 Benefit sharing can take many forms: the most tangible is often the sharing of financial benefits from research with research participants, which occurs at the level of individuals; but there can be many other types of benefits which may have a wider scope beyond the individuals who directly participate in research. These might include developing capacity and infrastructure, increasing skills and knowledge, and providing wider career opportunities and exposure to research stakeholders. Better access to healthcare and/or improved health facilities and advances in the types of healthcare available are all benefits that can reach the wider populations where research has taken place (table 1).

To date, individual research participants in the global South rarely experience benefits from the research in which they participate.10 Recent Ebola virus outbreaks in West Africa and the current global SARS-CoV2 pandemic have starkly highlighted this in Africa: Samples from Ebola patients appropriated by teams from the global North were used for commercial development without consent or benefit sharing agreements with countries, communities or patients of origin6 11; and COVID-19 vaccine scarcity and delays in access for adults in Africa persist in the face of booster shots for adults and child vaccination in the global North despite willing African participation in COVID-19 vaccine research and trials.12–14 Allegations of misuse of African DNA for unconsented commercial applications with unshared benefits persist.15 Ethics dumping, whereby foreign researchers undertake research in the global South under lower ethical standards than would be tolerated in their home countries, is still common10; and predatory, or ‘helicopter’ research in which foreign researchers fly in to collect samples, often treating local collaborators as sample collectors and excluding them from participating further in the research process, is still practiced across the global South.16 Experiences of inequitable research practices often underlie distrust in research by individual participants through to communities (eg, Havasupai,17 San10 and First Nations Australian18 communities), institutions and at national and regional levels.19 Similarly, researchers in the global South are also often distrustful of collaborations with global North institutions, although they may need to engage in such alliances to access research funding.20 Inequitable and/or neocolonial practices and power imbalances still underpin many ongoing research interactions between the global North and global South.21–24

In an effort to improve such practices, various communities and populations have set up requirements and guidelines for researchers who wish to engage with them, for example, the Te Mata Ira Guidelines for Genomic Research with Māori in New Zealand,25 The San Code of Research Ethics,26 27 and recommendations for research engagement with North American Indigenous groups.28 Regional guidelines increasingly enshrine more equitable research that includes benefit sharing, such as the African Academy of Sciences Data and Biospecimen Governance Guidelines.29

Onward data sharing has achieved global attention, and is normally a requirement to receive funding and publish research while benefit sharing mostly remains an afterthought: funders, journals and ethics review boards require data-sharing statements without asking for benefit sharing statements or plans; data sharing is often enforced, even where inequality might compromise the interests of those collecting the resources,30 and yet benefit sharing does not receive even a fraction of this attention. Community opinions on providing benefits and payments to participants commonly focus on financial benefits and elaborate on fairness of compensation, particularly for participants with very limited resources.31–33 In order for benefit sharing to be fair, considering proportionality is also important in terms of the benefits accruing to meso and macro-level stakeholders, who may take smaller relative risks compared with exposure to direct personal risk experienced by individual research participants.9

What can shift this unfortunate status quo? Increasingly, researchers in the global North are becoming sensitised to global inequities in research practices and showing increased willingness to engage with benefit sharing concepts.34 Currently, this is largely abstract engagement with limited translation of the concept of ‘benefit sharing’ into a clear strategy to encourage more equitable practices. The process of operationalising benefit sharing requires involving a wide range of stakeholders, beyond just researchers and participants, in normalising and inculcating benefit sharing in research undertaken in the global South. It requires advocacy with ethics review boards, peer-reviewed journals and research funders as well as ongoing consultation with participants and their communities about what might be acceptable benefits, beyond remuneration, in return for research participation.

A framework to guide operationalising benefit sharing in research

Taking the next step towards routine implementation of benefit sharing requires practical guidance on how benefit sharing might be implemented. Towards this goal, we present a benefit sharing framework that provides researchers with a practical resource to help identify ways to share benefits during health research (table 1). The development of this framework has been informed by the shared experiences of the authors undertaking research in the global South and participating in various health research consortia and networks with strong ethics components as well as capacity development programmes.

The framework is defined by two dimensions, namely Categories of Benefits, and Stakeholders. It is intended to provide an overarching structure to assist with identifying benefit–sharing opportunities, and could be applied across a variety of different contexts and health research domains informed by domain-specific experience and knowledge.

Exemplar matrix and case study

To illustrate the application of the framework for benefit sharing in health research, we present an applied example by populating a matrix that identifies a variety of stakeholders who could benefit from health genomics research in the global South, and describe different types of benefits that they might realise using the framework benefit categories (online supplemental data file). In the matrix, we provide some practical examples of how benefit sharing could be implemented to benefit microlevel, mesolevel and macrolevel stakeholders using the example of genomics health research, recognising that the matrix may not identify all stakeholders and opportunities for benefit sharing, but instead presents an evolving set of scenarios to assist and enable practical application of benefit sharing while conducting health genomics programmes undertaken in the global South. It is our intention to illustrate how researchers might use this framework at the planning stages of their own programmes to identify important microlevel, mesolevel and macrolevel stakeholders, and consider for each the benefits that might be created and shared under each category. It may also assist funders and ethics review committees in how they operationalise an intention to inculcate benefit sharing in research practices, and how they might assess benefit sharing plans in ongoing research.

In addition, we present a case study using the framework as a guide to assess benefit sharing at microlevel, mesolevel and macrolevels in COVID-19 research within Africa during the current pandemic, discussing successes, missed and future opportunities for benefit sharing (box 1).

Conclusion

In identifying different types of benefits that might be shared, it is essential to consider that individuals and their communities may have a wide range of motivations for participating in research, and may have different priorities with regards to the type of benefits anticipated as well as who will accrue them. Research programmes conducted in the global South, especially those funded externally and by the global North, would be well advised to engage meaningfully with each community involved in health research to understand where some of these local and individual priorities might fall, recognising the autonomy and self-determination of global South research participants in defining the terms of their preferred benefit sharing arrangements. Global North researchers will do well to consciously move from doing benefit sharing at global South participants towards building benefit sharing programmes with those stakeholders.

We have presented here a framework that can be used as a practical tool to identify ways of benefit sharing that extend beyond financial benefits provided directly to participants and patients at the point of interaction in research programmes, and rather recognise a wider range of potentially less-tangible benefits that can be extended to a variety of stakeholders. Many of these benefits may already be reaching stakeholders through more ad hoc routes in ongoing research programmes, but we believe that adopting an intentional and purposeful approach to identifying and enabling this kind of benefit sharing can help to operationalise existing intentions to undertake benefit sharing during research. When designing a new research programme, the researchers can use this framework to construct a benefit sharing matrix for their project—where needed, referencing the example matrix for health genomics research provided here as supplementary data, to assist in imagining practical ways to benefit share. In this example, we have used the health research benefit sharing framework to populate a matrix with stakeholders and types of benefits that could be shared in health genomics research in Africa. For these stakeholders we have identified types of benefits that might result from health genomics research, providing examples where those are already available.

In addition, scientific journals, funders and ethics review boards can assist with inculcating benefit sharing in research programmes through requesting benefit sharing plans and statements for all research projects, and this framework can similarly inform approaches to requiring and reviewing benefit sharing plans alongside data-sharing plans in research proposals and published manuscripts.

In developing our case study (box 1), we fully recognise the critical need for expediency in assessing transmission modes for the SARS-CoV-2 virus, and in developing and implementing vaccinations to curtail the severity and spread of the virus. As such, soliciting community input at all stages of the epidemiological, modelling, vaccine development and even translational studies for vaccine distribution lacked optimal public and community-specific input. Further delay in processes to ensure wide-spread input on community perspectives and preferences could have resulted in increased morbidity and mortality. However, in planning for future public and global health crises and to promote full consideration of community preferences and to optimise benefit sharing, investigators, providers, funders and policy-makers should foster such partners early on so these relationships are well established before there is a pressing need. The case study illustrates that a variety of benefits—which were identified by considering the types of benefit sharing in the framework—could be shared with microlevel, mesolevel and macrolevel stakeholders at many touch points during the COVID-19 pandemic, and that inculcating benefit sharing in everyday research practice could ensure that benefit sharing opportunities are utilised even in times of crisis. It also shows that the failure to consciously share benefits of scientific progress with the general public, at the micro level, has impeded public support for evidence based, scientific responses even while benefits have accrued to meso and macro stakeholders.

Had we already had true community-engaged partnerships before the start of the COVID-19 pandemic, the scientific community would have had greater insight into the perspectives of diverse populations, which may have resulted in decreased vaccine hesitancy. Taking a prospective approach now that considers ongoing benefit sharing, including bidirectional knowledge and skills sharing, can ensure that the voices of global populations are heard regarding scientific advancements that directly and indirectly affect them, and that scientific teams are well poised to ensure promotion of equitable benefit sharing for all, especially during times of public and global health crises.

This benefit sharing framework is a work in progress, and we anticipate that it will continue to evolve with input from interested parties and as benefit sharing becomes inculcated in health research, especially when it is undertaken in the global South. We invite and welcome comments and conversations towards this evolution from all interested parties.