Keywords

Area of Risk of Exploitation

This case study is about the conducting of genomic research on a vulnerable population, and it focuses on the enhanced need for respectful and authentic prior informed consent . While the research itself is undoubtedly of potential benefit to humankind as well as the participant population, the particular risk of exploitation lies in the fact that certain types of information gleaned from genomic research are essentially of a sensitive and private nature, and their publication can result in potential embarrassment, discrimination and collective psychological damage. The informed consent allegedly gained for this complex research project from the illiterate San participants was never disclosed to the San leadership, and, as is made clear below, the nature and content of the research publication was indeed damaging to the community on various levels.

Specific Case and Analysis

The general population of San peoples of southern Africa is known to carry the oldest human DNA on earth, and is consequently much sought after for population-wide genomic research aimed at understanding aspects of human evolution. The San peoples, known to be the earliest “hunter-gatherer” populations of southern Africa , number an estimated 100,000 individuals spread across at least five countries, with the largest populations in Namibia , Botswana and South Africa . Since 1986 the seven dominant linguistic groups have formed elected organizations in each country aimed at representing and protecting the rights of their illiterate rural populations. One of the most important roles of the San councils of Namibia, Botswana and South Africa is to protect their people from unwanted, inappropriate or exploitative research.

The stated purpose of the genomic research project under discussion was to sequence the genomes of four selected San individuals, and to “characterise the extent of whole-genome and exome diversity amongst them” – that is, the four San and a man of Bantu extraction. In addition it set out to “compare the described variants to known data-bases” in order to pinpoint genetic variations in genome-wide data , and to “facilitate inclusion of southern Africans in medical research efforts” (Schuster et al 2010).

In about 2009 researchers associated with the three universities began the process of obtaining informed consent and taking DNA samples from four selected San elders from three linguistic groupings, described as Tuu,!Kung and Ju/’hoansi. How the researchers communicated the methodology, aims and objectives of the complex research project via translators to the four illiterate elders will perhaps never be known: the San leadership later formally requested access to this information, but were refused. According to the published research, “all participants consented … via video-recorded verbal consent (Bushmen) ”. In February 2010 the research was published − to wide publicity in the popular media − in an academic paper entitled, “Complete Khoisan and Bantu genomes from southern Africa” , which was accompanied by a document containing supplementary information (Schuster et al 2010).

The acting regional coordinator of the Working Group of Indigenous Minorities in Southern Africa (WIMSA) , Ben Begbie-Clench, approached the paper’s authors requesting details of the informed consent process, as set out below. Mathambo Ngakaeaja, deputy director of WIMSA, subsequently wrote to Nature on 18 February 2011 objecting to the publication by Schuster et al., and describing how central the concept of prior informed consent was to all research affecting indigenous peoples . After commenting critically on the persistent refusal of the researchers to approach the official San leadership structures or engage meaningfully with them, Ngakaeaja stated that the purpose of his letter was “to draw attention to the absolute arrogance, ignorance and cultural myopia that is present here” (Ngakaeaja 2011a). He continued, “these researchers have basked in the glory of their publication whilst claiming smugly that they complied fully with the ethical requirements”.

From the perspective of the San leadership, many aspects of this research study were deeply problematic, and would have been objected to if one of their organizations (e.g. WIMSA, the South African San Council or the South African San Institute) had been given an opportunity to consider the research before it began or to approve the final form of the document prior to publication .

The San leaders engaged respectfully with the researchers following publication, requesting details of the informed consent process . Despite much correspondence,Footnote 1 the authors persistently refused to acknowledge the need to consult with San leadership or to provide details of the informed consent documentation or process.

We set out below some of the San leadership’s reasons for regarding the research project as exploitative .

Terminology

The use of words such as “Khoisan” and “Bushmen” and “hunter-gatherers” shows a lack of consultation with San leaders. All of these terms were freely used in the publication , but all are considered sensitive and problematic for different reasons. For example, the San object to being referred to collectively as “Khoisan” , a descriptive term coined by anthropologist Leonard Shutze in 1928 as a way of referring to Khoi pastoralist and San hunter-gatherer groups collectively (Schlebusch 2010). The word “Bushman”, meaning “uncivilized people”, is widely regarded as pejorative in certain contexts. The anthropologically loaded term “hunter-gatherer”, frequently used in the paper and the supplementary information, implies a generally acknowledged low social status (Wynberg et al 2009). Consultation would have resulted in more acceptable uses of these and other terms.

Published Conclusions Far Removed from Genomic Research

Much of the discussion in the supplementary information document related to terms and concepts such as “hunter-gatherer” , the low status of “hunter-gatherers”, the payment of lobola and dowry, and marriage practices, for example:

A feeling of inferiority associated with the “Bushmen” or “San” ethnic classification meant that many Bushmen women tried to uplift their status via marriage to Bantu men (Schuster et al 2010: suppl 3).

These conclusions could not have been drawn from the results of the genomic research, nor could they have been permitted by a process of informed consent to the collection of genomic data . The publication thus draws on and publishes conclusions drawn from other sources and disciplines, which would not have been permitted in a normal research consent process. The bad practice and injustice of publishing information that could not have been envisaged by the participants at the time of their giving consent would have been lessened had the authors returned to the communities before publication and tried to explain the far-reaching and sensitive nature of their findings. The San leadership, however, are unaware of any attempt by the researchers to return to the communities and explain the complex nature of the published conclusions.

Individual Versus Collective Consent

It is well known that indigenous, rural and illiterate people do not understand individuality and individual rights in the manner of the West, their identity being deeply collective and associated with their communities. This research project only obtained informed consent from the indigenous individuals who participated, while it is known and accepted that genomic research by its very nature speaks to collective issues. There is no shortage of published research ethics guidelines (e.g. NHMRC 2003, CIHR et al 2014) that set out absolute requirements for research on indigenous peoples , one of which is that collective “permission” should be obtained from the leadership, in addition to normal informed consent obtained from individuals. Not to do so is perceived as an expression of lack of respect for the community . However, one of the authors wrote to WIMSA saying, “As we are dealing with individuals in a personal manner (via their DNA) the individual has a right to participate or not as the information contained is of direct impact to that person” (Hayes 2011). This response does not take into account that genetic information also has a direct impact on family members of the participant.

Lack of Respect for or Reference to Indigenous Research Protocols

The need for “respect” to be shown to the particular community is perhaps the most important fundamental element in the indigenous research ethics guidelines referred to above. The requirement takes many forms, but can be summarized as authentic communication with the community leadership from the inception to the conclusion of the research project. None of the established suggested methods for showing respect to communities were employed in this case. The authors refused to consult with the leadership afterwards, relying upon the fact that allegedly none of the elderly and illiterate San participants had demanded to be represented by the San leadership. For that reason, they concluded that the San leadership had no say in the matter (Hayes 2011). This reliance on individual consent by an illiterate person who could have no idea of how the implications of genomic research related to the collective was and is regarded by the San (an abuse of power).

Failure of Research Ethics Committees/Institutional Review Boards

The researchers defended their methodology regarding consent and other aspects of the process by repeating that the project had been approved by no fewer than four separate research ethics committees . Yet not one of these committees referred to the published research guidelines on indigenous populations, which were readily available and with which they ought to have been familiar, despite the fact that the very purpose of the research was to examine the most famous of indigenous “hunter-gatherer” communities. In the words of Prof. Vanessa Hayes, geneticist and co-author of the Nature paper, these committees were formally designed to “approve, monitor and review biomedical and behavioural research involving humans with the aim to protect the rights and welfare of the research subjects” (Hayes 2011). In addition she stated that it was their duty to respect the “culture, dignity and wishes of subjects”. It is the San view that they failed dismally in this duty.

Breaches of Privacy in the Findings

The paper and its supplementary information included a number of discussions and conclusions that contained intimate, personal or pejorative information. The following are some examples discussed in the context of “Bushmen-specific phenotypes” (Schuster et al 2010: suppl 8): namely, how different genetic and environmental influences come together to create an organism’s physical appearance and behaviour.

  1. 1.

    “ Hunter-gatherer” associated with low social status: Commentary in the paper on “traditional life-style” included the following, which contains far-reaching and unsupported assumptions:

    A feeling of inferiority associated with the “Bushmen” or “San” ethnic classification meant that many Bushmen women tried to uplift their status via marriage to Bantu men (Schuster et al 2010: suppl. 3).

  2. 2.

    Lactase persistence: The following conclusion was drawn:

    As expected for a foraging society, we found the Bushmen in our study all to be homozygous for the C-allele, suggesting an inability to tolerate milk consumption as adults (Schuster et al 2010: suppl 4).

  3. 3.

    Human pigmentation: Conclusions were drawn about levels of San melanin pigmentation, their susceptibility as a group to skin cancer, and their consequent selective advantage for survival in the Kalahari desert (Schuster et al 2010: suppl 5).

  4. 4.

    Lipid metabolism and bitter taste alleles: Complex conclusions were drawn relating to Bushmen digestive tracts, and also the ability to sense a bitter taste, a trait which would potentially assist human survival in the wilds. The “taste receptor gene” was also discussed in the context of human evolution from Neanderthal to the present (Schuster et al 2010: suppl 7).

  5. 5.

    Genes related to hearing: Drawing on the findings, the paper indulged in speculation that “Bushmen have better hearing than Europeans” (Schuster et al 2010: suppl 8).

Lessons Learned

The San leaders see the Schuster case as a telling example of the harm and disrespect that research can bring about, notwithstanding approval by ethics committees/institutional review bodies. It also highlights the need for San themselves to create their own protection mechanisms.

With this in mind, the San held a consultative workshop in September 2014 comprising San leaders from Botswana , Namibia and South Africa , as well as genomic researchers, ethicists and lawyers. The purpose of the workshop was to discuss the San’s perception of the exploitation inherent in the approach followed by the Schuster research, and to propose a San response to ensure that such research could never take place again.

In 2016 the San held two further workshops under the auspices of the TRUST projectFootnote 2 designed to take the earlier discussions further and to consolidate proposals aimed at ensuring that the San could in future manage and control research being done on their communities. These proposals are set out below.

Recommendations

The following recommendations emerged from the San workshop aimed at preventing exploitation in research.

  • Collective permission must be obtained for all research to be carried out on San individuals or communities.

  • The San Council is the elected organization in South Africa mandated to engage in this process with researchers.

  • The San have since developed a San Code of Research Ethics (San Council 2017) that has to be completed by all prospective researchers. This code contains a number of requirements relating to the need for research to be both respectful and useful to the San peoples, including:

    • early identification of research useful to the San

    • joint development, where appropriate, of design, content and methodology of all aspects of the research

    • full details provided in advance of all aspects of the research, including (potential) benefits to the San

    • commitment to pre-publication consultation , where appropriate, and post-publication feedback to the community