Anatomists' uses of human skeletons: Ethical issues associated with the India bone trade and anonymized archival collections

Concerns have recently been expressed about the continuing availability of human bones from India, obtained originally for educational purposes but lacking the requisite informed consent that would be expected today. More generally, a broader claim is being made, namely, that the practice of using any unconsented bones in educational settings is unethical and should cease. These calls, in turn, raise broader issues regarding the availability of anonymous archival collections in anatomy museums. Although this debate centers on undergraduate anatomy teaching, much anthropological research utilizes human remains of past populations for which there can have been no consent. A suggested alternative for undergraduate teaching is the use of 3D images of human bones, rather than the bones themselves. In addressing these issues, the background to the India bone trade is assessed, and the year 1985 is pinpointed as having significant ethical weight. The cultural and ethical interests inherent in studying archival anonymous skeletal material are weighed against indiscriminate reburial. Although any use of unconsented material represents ethical compromise, account should be taken of changing ethical expectations with time. It is concluded that: there is no justification for repatriation or disposal of all bones for which specific informed consent has not been obtained; continued use of anonymous archival human bones in a professional setting is acceptable, even in the absence of informed consent, with the proviso that there are no culturally relevant groups seeking repatriation; the continued existence of bones in long‐standing private collections cannot be justified since it amounts to long‐term storage with no identified goals; the notion that 3D images are an ethically superior alternative to actual human bones is unsustainable, since there is an intimate connection between the bones and the 3D images.


INTRODUC TI ON
There has been a flurry of concern of late over what is described as "skeletons in the closet," referring to the use of human bones originating in the main from the once active and accepted trade in human skeletons from countries such as India, for undergraduate medical education. There has also been a call for an end to the use of actual human bones in educational settings. 1 This is a long-established practice integral to the education of medical and other health sciences students. It was legal and no concerns were raised about any ethical impropriety at that time. Those were unenlightened days, long before ethical concerns were raised about their origins and whether they involved any dubious practices.
It was common practice for medical students in Western countries to purchase boxes of half skeletons, as did the author in London in the 1960s. 2 They were purchased from reputable and longestablished companies, that in some cases are still in existence and continue to trade in a wide range of anatomical models and related products. 3 This does not justify the practice, but it puts it into its historical and cultural context. And this was far from an isolated practice that today would be considered ethically dubious. Think of the dissection of unclaimed bodies, or obtaining brains from pathology postmortems, neither with informed consent nor with the next-of-kin's knowledge. 2,4,5 Think, too, of anatomy museums with, in some instances, skeletal material, embryos, and fetuses stemming from eras pre-dating modern ethical discernment, once again lacking informed consent. [6][7][8] It is this melee of ethical debate that provides the context for approaching the continued existence and use of human skeletons in both private and institutional collections deriving from the latter part of the 20th century and earlier. This is not a new debate, and neither is it a novel phenomenon, no matter how confrontational in the eyes of some.
In reflecting on these calls for an end to the use of human bones, four possibilities emerge. These are: (1) repatriation or disposal of all bones for which specific informed consent has not been obtained; (2) continued use of anonymous archival human bones in a professional setting, such as Anatomy departments or equivalent educational institutions, even in the absence of informed consent; (3) continued maintenance, and possibly use, of bones in long-standing private collections; (4) replacement of actual bones in all these situations with 3D images of bones, on the ground that this is the sole ethical course. Each of these raises a range of ethical issues that will be addressed in the following sections.

S K ELE TON S IN THE CLOS E T AND THE INDIA BONE TR ADE
Coman and co-workers 1,9 have called for an end to the use of actual human bones and have urged authorities to develop legal and ethical pathways for their disposal. Their dominant concern appears to be that there remain large numbers of human bones in private collections, and that these may continue to be passed from one generation to the next. It is contended that, in the absence of valid informed consent, this confounds the core ethical principles of autonomy and justice. The holder of the bones, so the argument goes, lacks consent to hold them or pass them on. 9 It is also argued that, since there are acceptable artificial options for use in medical education, namely, 3D printing, the continued use of actual human bones is difficult to justify. 1,9 While it is private collections that are the prime focus of these objections to the use of actual human bones, the arguments are more extensive than this, with a call for all bones to be replaced with artificial alternatives.
Since it was the India bone trade that provided the bulk of the bones used in medical education in Western countries, this trade is central to this debate. In clarifying the nature of this trade, a distinction needs to be made between the pre-and post-1985 trade, since most of the bones in private hands emanated from those purchased by medical students before the mid-1980s. This was a legitimate trade in Western countries, with students purchasing bones from recommended osteological companies. In the 1920s and 1930s, these companies had purchased bones and skeletons from France, Russia, Germany, and India. 3 From 1937 onwards India became the principal supplier and was built on a relationship established between one of the owners of the United Kingdom company and a major distributor in Kolkata. Notwithstanding the quasi-legitimacy of the trade, the bones were derived from the lower castes who were economically disadvantaged and were pressured to sell the bodies/bones of their loved ones. The degradation of these populations was far removed from the respectability of those selling and purchasing the bones in Western countries. The trade came under scrutiny in the late 1970s and the export from India was banned in 1985 by the Indian government. 10 In the early 2000s, the buying and selling of human skeletal material were prohibited in many countries, for instance, in the United Kingdom (Human Tissue Act 2004 11 ).
In recent writings, India's underground bone trade has been severely criticized, although much of the criticism has been directed at the trade being undertaken after 1985. 12 The conditions described are deplorable, and the ethos has much in common with that associated with the body brokers in the United States. 13 Both are unethical and should be resolutely opposed. There can be no justification for any black market along these lines, based as they are upon greed and inequity, and medical schools outside India that utilize such sources are acting unethically. This recent bone trade is akin to the use of unclaimed bodies for dissection with its lack of informed consent and disrespect toward the deceased and their families. 5,[14][15][16][17] But what about the earlier trade, which accounts for the bulk of skeletons found in Western Anatomy departments?

BACKG ROUND TO THE IND IA BONE TR ADE
The pre-1985 bone trade was on a par with the acquisition of bodies prior to the 1832 Anatomy Act in the United Kingdom and its equivalent in other countries. The 1832 Act came about due to growing societal repugnance at the unscrupulous behavior of anatomists in obtaining bodies for their medical schools. 5,[18][19][20][21] The Act itself did not bring about acceptable standards as are practiced in the late 20th and early 21st centuries since unclaimed bodies continued to be the primary source of bodies for well over 100 years. However, it did begin the long process of setting standards for the way in which bodies are obtained, governed by ethical thinking and ethical debate. Even today there is a long way to go before body donation is established worldwide, but a trajectory has been set. [22][23][24] It is against this background that the acquisition of bones and skeletons should be assessed. Discussions regarding the means of obtaining human skeletons are at a far more preliminary stage, and it has taken the publications of Coman and co-workers 1,9 to bring this to the attention of the wider anatomical community. In reply, Cornwall and co-workers 25 , while agreeing that repatriation policies for privately held bones are needed, argue against the view that all non-consented anatomical specimens should be destroyed. This is because they are tangible legacies of the past, that can be used to elicit discussion on contemporary ethical and professional practice. 26 They form a valuable legacy, because the activities of anatomists in the past, utilizing the best ethical understandings of the time, should not be ignored. Apparently, the skulls that are provided would otherwise be discarded or destroyed.
It is indisputable that an adequate ethical rationale is required for the continued use of bones sourced from India. This is because any use of unconsented material is a compromise, and the argument here is that the year 1985 should constitute a tentative benchmark. The pre-1985 trade appears to have been con- Should the lack of consent prior to 1985 be sufficient to disbar continued use of this material, leading to the related question of what would then be done with the material? Is its disposal ethically superior to its continued use in teaching and or research in the health and social sciences with proper historical accounting? These questions parallel those raised by the continued use of anonymous archival material in anatomy museums. 7 Ethical equipoise is to be sought, between burial even when there are no individuals or cultural groups requesting this and continued use of potential benefit to current students and researchers in the health and social sciences.
Human skeletal material from pre-1985 India is anonymous and archival and is being used in ways that enhance teaching, and that are educationally valuable for future health science professionals, and their clients. The ethical balance is weighted toward use rather than disposal, with the proviso that such unprovenanced material is not treated as 'the Other'. 28 Since there is no way of building up trust with the communities in India from which the skeletons came, the ethical challenge when used in teaching and research is to create awareness that the bones were from human individuals who almost definitely belonged to disadvantaged communities. These ethical strictures are never to be subordinated to the immediate demands of learning basic anatomy, important as the latter is. Repatriation is not a viable alternative, and burial is not an ethical necessity; nevertheless, ethical care remains a prerequisite.

MUS EUM COLLEC TIONS
Many Anatomy departments are characterized by museums containing a large collection of human material that originated in the distant past. Such anonymous archival material would have been collected from numerous sources from the 19th century onwards. It has no known links to its original subject, little or nothing may be known about the method of acquisition of the tissue, and it is highly unlikely that there would have been any consent. On the assumption that any human material, regardless of its origins, is to be treated with respect, efforts are to be made to determine whether there are any family members with an interest in the material. Even when there is no such known interest, the collections retain historical and educational value, and it is this that is to be the determinative factor in deciding on its retention or disposal. 29 In contemplating the range of options available for dealing with anonymous archival human material, four have been assessed. These are the quadrilateral of destruction, teaching, research, and indefinite storage. 7 An additional fifth option, skeletonization, is raised in the section, Skeletonization procedures.
The first option of destruction is disposal through burial or incineration as clinical waste. This does not directly benefit any of the parties currently interested in the material, although theoretically, it protects the material from any perceived misuse in the future.
The material exists and hence something must be done with it. In the author's view, disposal is not an ethically neutral action since it presupposes that disposal is preferable to any other possible use. 30 It will not benefit members of the human community and may be regarded as a waste of human resources. On the other hand, if the material resulted from flagrantly unethical actions, as during the Nazi holocaust, the only way in which respect can be shown is to bury the material. 31 A related illustration is that of the presence of the remains of enslaved individuals, for example, in the Peabody

Museum of Archeology and Ethnology, and the Warren Anatomical
Museum, at Harvard University. 8 In both these cases, the society was implicated in their demise and subsequent availability for anatomical and anthropological study. Burial of all such material is a legitimate response, but will not apply to most human skeletal material encountered in most Anatomy museums. Neither will it apply to most skeletons from India, even if the availability of the skeletons reveals an underbelly of an unjust society.
The use of anonymous archival material in teaching produces immediate educational benefits. The teaching rationale should be a focused one and should be based on clearly articulated teaching goals. 7 This option is the one of greatest relevance to the question of the use of skeletal material originating in India and purchased years ago for educational purposes. Much of this material has been passed to Anatomy departments over a prolonged period and has been integrated into the anatomical collections used principally for teaching undergraduate health science students. Ethically, its use in teaching is superior to its disposal, if the only reason for the latter is that it should not exist.
The third option is for the skeletal material to be used in research.
The justification in this case depends upon its potential usefulness in providing insights into clinical conditions, and the possibility of benefitting future patients. Benefits such as these are far from assured, but they are a start. There is no doubt that well-provenanced skeletal material offers far more incisive opportunities for profitable research ventures, than does the use of unprovenanced material.
Nonetheless, both have much to offer, as demonstrated by the work of biological anthropologists. 32 The fourth option is that the material remains in storage on the ground that it may prove valuable in future, yet to be determined, research projects. This is a dubious option ethically, since it has overtones of the mere stockpiling of tissue, but it cannot be categorically dismissed due to the burgeoning potential of genetic analyses. 33,34 A sound research rationale must include potential realistic future benefits to science and medicine.
The indelible gold standard is undoubtedly the use of human material for which specific consent has been given for its use in teaching and research. Hence, the use of unconsented archival material is always a compromise and should never lead to a diminution in the respect shown to the human body and its parts.
Routinely, it is preferable to err on the side of altruism, and hence for consent for the use of all newly acquired human material. This is not possible with anonymous archival material since there were no voluntary donors, and this includes skeletal remains handed into anatomy museums. Nevertheless, archival samples should be treated with equivalent care and respect to that shown consented donated human material from known donors. This stems from the view that those in charge of human material are to act as its custodians rather than its owners, shouldering responsibility for every aspect of its welfare. The use of unprovenanced material should be treated with considerable care and with awareness that this is sensitive ethical territory.

RE S E ARCH US ING HUMAN S KELE TONS
The emphasis up to this point has been on human skeletal material in undergraduate teaching. When the research is in clinical anatomy, it will generally be focused on material that has been specifically donated to a medical school for teaching and research. Nevertheless, there are exceptions to this general rule, and this is where specific known individuals were wronged. Over the years conflict has erupted over the continued display of Charles Byrne, the 'Irish Giant,' whose wishes for burial at sea were over-ridden so that his skeleton could be retained for examination and display on his death in 1783 until very recently. [41][42][43] Another example was that of Sara Baartman, the 'Hottentot Venus' in the early 19th century, when dissection of her body was carried out in a 'racist' fashion. 44,45 Each of these raises a different set of issues, but all point to the significance of enquiring whether there is an ancestral link or continuity of beliefs between the individual in question and researchers and museums today. Legitimate concerns have also been expressed over the retention in American museums of the remains of enslaved individuals, reflecting as they do the societal values that led to the treatment of slaves during life and at death. 8 In this instance, there is a conceptual link between attitudes toward the owning and treatment of slaves postmortem, and benefits accruing today from these practices for anatomical study.
A fundamental premise is that our respect for the beliefs and There is also information to be gleaned on how communities were organized, what technologies were available, and the cultural practices of social groups. 46,47 An example is provided by research conducted on a Church burial ground in New Zealand, where a study was conducted into early settler graves in the region. 48 The cemetery was used be- The other scenario stems from the late 19th century when two 'headhunters' took skulls from the ruins of a medieval monastery in Galway in Ireland. 50 The skulls were of ordinary parishioners and had been kept at the monastery for safekeeping. They were ultimately removed to the Anatomy Department at Trinity College Dublin, as representatives of the Inishbofin, characterized as a group of 'primitive' people. The skulls were measured in the belief that craniology could shed light on the intelligence and development of different races. In this instance, the rationale for keeping the skulls is doubly problematic: the research is now discredited, and there are living descendants who want them returned.
Research has its own justification, as well as its own ethical strictures. The lack of consent by the original peoples does not invalidate undertaking research on bones that have been incidentally found or actively sought as part of research projects. What is ultimately done with the bones following the research will vary depending upon a host of circumstances. The important point for the present discussion is that the lack of informed consent is not the sole determining factor and should not be wielded as the ultimate argument for disposal. If there is uncertainty about the ethical acceptability of the way the bones were obtained, that uncertainty flows over to the 3D images that are also ethically tainted. 52 The natural and the simulated cannot, in ethical terms, be hermetically sealed from one another. There are good practical reasons for producing 3D images of human material and human tissues, 53-55 but they do not constitute a means of by-passing ethical quandaries.

THE ALTERNATIVE PROVIDED BY 3D IM AG E S
Previous discussion of ethical issues surrounding 3D printing concentrated on creating images of body parts, and therefore on issues raised if these were produced from unclaimed bodies. 52 The 3D approach is not the sole alternative to employing natural/real human skeletal material. Think of replica skulls, spines, pelvis, long bones, and very extensive ranges of anatomical models covering every aspect of the human body's organization. 3 Virtual anatomy software provides close-up visualization of anatomical structures, resulting in an appreciation of the spatial relationships between anatomical structures. Additionally, there are interactive 3D models and simulations, although in the main these are directed at replacing or enhancing dissections. None of these are directly relevant to the replacement of actual human skeletal material.

CHANG ING E THIC AL E XPEC TATIONS
Every aspect of this debate hinges on one fundamental understanding, and this is that ethical expectations change with time and cultural mores. This does not allow present-day anatomists to accept deeply unethical practices in the past, but it does point to a readiness to take serious note of procedures that are unethical by today's standards. It is also a signal that current ethical expectations need to be open to adjustment as further insights arise. Alongside this, it forces today's practitioners to consider how best to correct historic wrongs, or at a minimum to address them and expose them to ethical gaze. Carter, collaborated on the project that was to result in the publication of Anatomy Descriptive and Surgical. 57 Gray was a researcher, and research was an important foundation for the work he did a short time later, on what was to become known as Gray's Anatomy.
The dissections were undertaken on bodies at St George's Hospital in London and would have been those of the poor from workhouses, prisons, and hospitals, whose remains had not been claimed by any family members. They were unclaimed, although since misconduct was rife and few formal records were kept, it was probably deception that led to some ending up in the unclaimed category. In these ways as well as in the scientific details, that first edition is worlds removed from the latest 42nd edition, 58 and yet that simply illustrates the wealth of developments that have taken place over 160 years or so.
Historian Ruth Richardson 59 has commented: "In Gray's, the legally sanctioned bodies of people utterly alone in the metropolis were the raw material for dissections that served as the basis for illustrations that were rendered in print as wood gravings. As massproduced images, they have entered the brains of generations of the living-via the eyes, the minds, and the thoughts of those who have gazed at them." (p. 139). Nowhere in Gray's Anatomy is their origin or predicament mentioned, an unsurprising observation for something written in the mid-19th century.
By today's expectations, the ethical world of Gray's Anatomy was very shadowy, and yet this was far from unusual for the time and culture in which these young anatomists were functioning. On the other hand, the limitations of that time are to be exposed and criticized as appropriate. Only in this way will the ethical environment of anatomy be improved, and the culture of anatomists be changed.

S KELE TONIZ ATION PROCEDURE S
The working assumption to date has been that there is no way of obtaining suitable skeletons ethically; hence, the four approaches of dealing as ethically as possible with unconsented material. However, there may be a fifth method, namely, accepting donors specifically for their skeletal material, with the skeletonization undertaken in-house. Few body donation programs currently have appropriate facilities to do this on a sufficiently large scale. Consequently, this proposal may be of limited practical relevance in the foreseeable future, and yet from an ethical perspective, it is worth serious discussion.
Envisaging a future in which such ethically-derived skeletal material might be available, it opens up a scenario where the unethically obtained material can be respectfully disposed. Any unique anatomical variation in the unethically derived skeletal material could be retained on account of its irreplaceable educational value.
A small amount of the old material can also be retained and used to educate users about the inappropriate and unethical manner in which these bones were collected in the past. This would allow anatomists to be transparent about the challenges of obtaining human material, and a means of pointing to the unethical ways that had to be employed in the past. The contrasting material would illuminate substantial ethical questions, namely, to discuss the use of consented versus non-consented tissues and to discuss the overall ethics of using human tissue.

CON CLUS IONS
In view of the preceding discussion, the four possibilities outlined in the Introduction can be considered afresh.
1. There is no justification for repatriation or disposal of all bones for which specific informed consent has not been obtained.
2. Continued use of anonymous archival human bones in a professional setting is acceptable, even in the absence of informed consent, with the proviso that there are no culturally relevant groups seeking repatriation.
3. The continued existence of bones in long-standing private collections cannot be justified since it amounts to long-term storage with no identified goals. 4. The notion that 3D images are an ethically superior alternative to actual human bones is unsustainable. This is because there is an intimate connection between the bones and the 3D images, so that if the former are thought to have been unethically obtained the latter will also have an unethical provenance.
A dubious ethical episode in one's anatomical past is an opportunity to reflect on what was readily accepted by a whole cohort of anatomists at that time. There is no way of eradicating that episode from any of our experiences, but subsequently, we have had many opportunities to change and learn. Were actual human bones essential for an undergraduate level of anatomy learning? The answer is probably 'no'. The array of simulations available today was not available 40 years ago, and whether they are sufficient by themselves, even today, is a question for the educationalists. If nothing else this points to a close relationship between educational objectives and ethical ones.

ACK N OWLED G M ENTS
The author acknowledges and thanks all those individuals, unclaimed, unidentified, unconsented, and those who willingly donated, whose bodies and bones have been used for education and