Barriers and Facilitators to Eye Donation in Hospice and Palliative Care Settings: A Scoping Review

Background: The need for eye tissue for use in sight saving and sight restoring surgery is a global issue. Approximately 53% of the world's population has no access to interventions such as corneal transplantation. Low levels of eye tissue impact on service providers such as National Health Service Blood and Transplant who aim to achieve a weekly stock of 350 eyes but do not meet this target. Aim: Patients who die in hospice and palliative care settings could be potential donors; therefore the aim of this systematic scoping review was to identify the potential for eye donation and barriers toward it from these clinical contexts. Design: A scoping review following the Joanna Briggs scoping review methodology was applied to search the global literature. Results: 13 articles from the global literature were retrieved. Evidence indicate that 542 patients could potentially have donated their eyes. Key barriers to increasing eye donation include the reluctance of healthcare professionals to raise the option of eye donation and the evidenced lack of awareness of patients and family members about donation options and eligibility. This review also indicates a lack of clinical guidance drawn from high-quality evidence proposing interventions that could inform clinical practice and service development. Conclusion: The scoping review presented here provides an up-to-date view of the current potential for, perceptions toward, and practice underpinning offering the option of eye donation to dying patients and their family members in hospice and palliative care context.


Introduction
The need for eye tissue is a global issue. Gain et al. 1 indicate that *53% of the world's population has no access to interventions such as corneal transplantation reporting that globally, only one cornea is available for the 70 that are needed. These data highlight an ongoing disparity in supply and demand for eye tissue in most countries worldwide. Furthermore, >2 million people in the United Kingdom are living with sight loss, which is predicted to increase to 4 million by 2050. 2 Corneal blindness is the fourth leading cause of blindness worldwide with an estimated 80% of all cases being avoidable and reversible. 3,4 Evidenced Barriers to Increasing Eye Donation International empirical data report that low levels of eye donation outside of Intensive Care Units and Emergency Departments 5-8 is due to negative attitudes toward eye donation held by health care providers (HCPs), [9][10][11][12][13] negative public views regarding eye donation, 14,15 and low levels of support on the Organ Donor Register (ODR). 16 Recent data indicate that 85% of registrants on the ODR indicated a willingness to donate all organs and tissues but of those who log a restriction, 68% decline eye donation. 16 Furthermore, recent data from U.K. Hospice Care settings 17,18 identified that the majority of staff had rarely or never raised the topic of eye donation with patients or relatives as part of end-of-life care planning.
Low levels of eye tissue have a direct impact on service providers such as NHS BT who aims to achieve a weekly stock of 350 eyes for use in transplant and other sight saving surgery, but current stocks are *150 eyes per week (personal communication with tissue services April 12, 2020). There is a need to achieve a sustained supply of eye tissue and as patients who die in palliative and hospice care settings could be potential eye donors, 2,19 this article presents a scoping review of the global literature that specifically looks at the barriers and facilitators to achieving eye donation from these settings.

Review Methodology
This scoping review followed the Joanna Briggs Institute ( JBI) framework for scoping review 20 (Table 1) and used the Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR) checklist to illustrate selection of the final included articles (Fig. 1). 21 Scoping review methodology was deemed appropriate to identify the scope, coverage, and type of research currently available on a topic, map the available evidence, and generate a synthesis of the available knowledge. [22][23][24] Review Question and Objectives Review question What are the evidenced barriers and facilitators to eye donation in Hospice and Palliative care settings?

Objective 1
To systematically map the current international evidence base relating to eye donation in hospice and palliative care settings.

Objective 2
To identify the factors that are evidenced as informing or influencing the option of eye donation being discussed with service users in hospice and palliative care settings.

Inclusion Criteria
The inclusion/exclusion criteria were developed in line with the JBI framework clarifying the Population (P) Concept (C) and clinical Context (C) (PCC), type of evidence sought, and other limiters within which the search was bounded ( Table 2).

Evidence Searching and Selection
An initial search was undertaken in the PubMed database using the terms ''Eye[MeSH] AND Tissue Donation[MeSH]'' ( Table 3). The search was limited to articles published during or after the establishment of the U.K. Corneal Transplant service. 25 However, the resulting 190 articles did not include several key articles known to the review team. Therefore, 23 articles (the development set) known to the review team and verified against the inclusion criteria were compiled and checked for indexing in PubMed.
Results showed that only five (28%) could be retrieved in PubMed. Seventeen of the 18 excluded articles were not indexed under the term ''Eye [MeSH] despite six of them having eye related terms in the title and/or abstract.'' MeSH or equivalent databasespecific terms were dropped for further searchers. Screening of title, abstract, and full article of the 190 articles from the initial search resulted in 70 articles being added to the developmental set of 23 articles previously identified, producing a test set n = 93 records. Finally, a two-stage process aiming to maximize the sensitivity of the search strategy and minimize the number of irrelevant records (specificity) was implemented. 26 Stage 1 applying search terms-''(eye OR cornea*) AND (donat* OR donor*)'' returned 10,313 records [retrieving 85 (91.4%) of the test set]. Stage 2 involved iterative stepwise identification and testing of exclusion terms (specified by the Boolean term ''NOT'') to exclude irrelevant records while maintaining the 91.4% level of sensitivity. The team used the PubMed PubRe-Miner tool 27 to identify potential exclusion terms (PubMed PubReMiner allows users to see frequency tables of occurrences of relevant terms from articles included in a given search, and their associations with other attributes such as topics or keywords). 27 We consulted specialist subject librarians at University of Southampton throughout development of the Defining and aligning the objectives and questions 2 Developing and aligning the inclusion criteria with the objectives and questions 3 Describing the planned approach to evidence searching and selection 4 Searching for the evidence 5 Selecting the evidence 6 Extracting the evidence 7 Charting the evidence 8 Summarizing the evidence in relation to the objectives and questions 9 Consultation of information scientists, librarians, and/or experts throughout search terms. 28 This strategy was repeated across five additional databases returning a total of 4322 records from all sources (Table 3).

Selecting the Evidence
The final screening process following the PRISMA-ScR framework for reporting scoping reviews 21 is illustrated in Figure 1 One hundred twenty-seven articles (of 140) were excluded: 14 records did not relate to eye donation (i.e., these contained only incidental references to eye donation, or did not include a significant focus on it); 28 did not relate to ''perceptions, preferences, views, attitudes, beliefs, experience, knowledge'' elements of our PCC, whereas 85 were not in the context of hospice and palliative care (as relevant articles often did not clarify this context in the title, abstract, or keywords). Thirteen records met the inclusion criteria and were included in the final review.
Extracting the Evidence Authors, aims/purpose; study design/methodology, participants/sample size, method of data collection and analysis, finding and limitations were extracted from the final 13 records and reported in Table 4. Studies listed in Table 4 are referenced in the text by numerals in square brackets.

Charting the Evidence
Thirteen records that met the inclusion criteria were exported to Atlas.ti 8 29 for management and analysis. Articles were analyzed in line with the review objectives.  [1][2][3]7,[9][10][11][12]. Five publications were retrieved between 2012 and 2020 [4][5][6]8,13]. Search results indicated that there has been an evidenced increase in publications linked to eye donation from palliative and hospice care settings since 2001. This may be in response to increasing awareness of the shortage of eye tissue for use in transplantation and medical research and the recognition of the potential for donation from these settings.
Participants. Sample sizes in the retrieved empirical studies ranged from 8 to 25 participants involved in semistructured interviews [1,2,4,5] and 11 to 704 respondents in surveys [3,6,8]. Publications reporting retrospective note reviews included between 84 and However, in units where donation was routinely discussed, participants generally consulted relatives rather than patients resulting in concerns that patients were not involved in decision making. Patients or family members ''openness'' to discussing end-of-life planning led to HCPs being more comfortable raising the option of donation. Discussing donation should be a multiprofessional role.
Timing of the discussion is crucial to the outcome.
A main concern was whether the request for donation and the donation process would cause the patients and families any physical or psychological harm. given the option to donate and later realized, they could.
Raising the topic of eye donation: discussions were initiated by nurses generally after the death of the patient. The timing and approach were acceptable to families although they felt it would have been easier if they had known beforehand.
Participants views of eye donation: Most participants felt that donation was right and had a positive experience with the process and felt they had done something worthwhile.
Social policy: 10 participants stated that the patient should make the decision about donation.
All participants felt that there should be publicity and discussion about organ donation preferably before the person was faced with incurable disease or imminent death.  Eyes were not perceived as being different to other organs and participants valued sight and felt it would be important to help someone see again.
All participants acknowledged the role played by their family in decision making and were keen to involve them. Participants felt they would prefer to talk about donation when they were well rather than when vulnerable and close to death. Participants felt discussions about donation was a covert way to tell someone that they were dying. Participants were open to discussing donation with healthcare professionals and felt it would be easier with someone they already had relationship with. Although participants said they did not know anything about donation, they, however, felt they would not be eligible to donate. Some thought they could pass on their cancer if they donated. Results of survey healthcare professionals: 92% (n = 92) of respondents never or rarely raised the subject of corneal donation with patients or relatives.
76% (n = 76) of respondents had not received any information or training regarding corneal donation.
81% (n = 81) of respondents felt they did not know enough about corneal donation to discuss it with patients or relatives.
Knowledge and training were identified as significant barriers to raising these discussions.
Results of questionnaire with inpatients: 6/11 (54.5%) participants had not heard of corneal donation and all were either glad or neutral about being informed about corneal donation. 8/11 (73%) participants did not find it upsetting to discuss corneal donation and the remaining 3/11 (27%) indicated although they found it upsetting, they would rather have a conversation than not.
Patients' decisions about donation changed after discussions of eye donation. Before discussion none of the patients were planning to donate their corneas, whereas after the discussion 7/11 (64%) were planning to donate.
(continued)  Patients often spontaneously discuss end-of-life matters such as their funeral arrangements, their will, and expectations for the time they have left, but they rarely spontaneously discuss organ or tissue donation. Introducing donation discussions increased donation rates.
Patients should be given appropriate information to enable them to make choices about donation.
Knowing the wishes of the deceased regarding donation influences next of kin donation decision making. Healthcare professionals find it challenging to talk about donation even though they frequently have difficult discussions about death and dying. HCPs are fearful of the reaction of patients and families to the request for donation.
The attitudes of healthcare providers influence their practice, those with negative views and less knowledge about donation are less likely to discuss it compared with those who are positive and have more knowledge.
HCP, health care provider.
None of the retrieved evidence reported participant characteristics such as gender, ethnicity, or religion. Of the two literature reviews, one focused on how healthcare professionals could impact on the number of eye donations from their clinical areas, outlining the potential benefits and considerations when involving patients in eye donation discussions [12]. The second focused on involvement of patients and family members in eye donation discussions [13].

Potential for eye donation
Findings from retrieved retrospective note reviews were conducted in one palliative care and four hospice care settings. Data from the hospice settings reported between 52/100 (52%) and 164/174 (94%) of deceased patients could potentially have been eye donors [6,[8][9][10] and in the palliative care setting the potential was 229/704 (35.2%) [11].
In aggregating data from these retrospective reviews, the potential for eye donation from hospice care settings was 313 and from palliative care settings 229. This suggests a potential donor population of 542; however, these figures relate to patients who were assessed as medically suitable to be eye donors, but we cannot extrapolate how many patients would have agreed to eye donation if asked. However, limited evidence suggests that discussions about eye donation can increase donation rates [6][7][8].
Summary: Objective 1. Mapping of the global literature retrieved little evidence exploring barriers and facilitators to eye donation from palliative and hospice care settings was available before 2001 and that a limited range of study designs/evidence synthesis methodologies had been adopted in the reported empirical work. Nine of the 13 publications were conducted in the United Kingdom with a dearth of literature from other countries and cultures. With the United States and India reportedly supplying 55% of all corneas available globally, 1 it is surprising that there is no literature from these countries.
Although the evidence available includes representation from relevant participant groups patients, family members, and healthcare providers, the sample sizes are frequently small; however, the themes generated by the retrieved publications speak to recurring barriers and facilitators. To date the available literature base is very slim with a lack of high-quality primary research adopting mixed methods of investigation/ exploration that would support practice and policy development.
Objective 2: To identify the factors that are evidenced as informing or influencing the discussion of eye donation in hospice and palliative care settings Analysis for Objective 2 focused on identifying factors that were evidenced as informing or influencing the end-of-life option of eye donation in hospice and palliative care settings applying qualitative content analysis. 30  Evidenced attitudes toward eye donation (including beliefs and perceptions). Attitudes is defined as a learned tendency to evaluate things people, issues, objects, or events in a certain way. 31 Evaluations are often positive or negative and informed by a person's beliefs and perceptions. 31,32 Findings in this section have been synthesized from four studies reporting the attitudes of healthcare providers [1,3,6,8], three reporting the attitudes of patients [4][5][6] and three reporting the attitudes of carers or family members [2,7,8].
Healthcare providers are reported to be generally favorable toward eye donation, perceiving it as worthwhile [1,3,6,8]. Authors report that although participants felt uncomfortable discussing eye donation, the majority felt it was their professional responsibility to do so [1]. Similarly, Gillon et al. [3] exploring attitudes, knowledge, practice, and experience of corneal donation across a sample of 410 HCPs respondents report that 70% (291/410) perceived corneal donation as a rewarding opportunity for patients and/or their families and 82% (345/410) reported that corneal donation was compatible with their personal beliefs [3].
Furthermore, survey findings [8] report that 42% (8/14) of doctors raised the issue of eye donation based on their experience that the option was perceived by patients and family members as a way of giving something back to society. Of note is that although HCPs acknowledge that eye donation is worthwhile, evidence indicates that discussing eye donation is not common practice [3,6,8,12]. Specifically, two surveys including HCPs found that 92% (92/100) and 93% (399/431) never or rarely raised the subject of corneal donation with patients or relatives [3,6].
Authors suggest that HCPs' perception that discussing eye donation will cause distress to patients and family members is a barrier to eye donation [1,3,8,12]. For example, retrieved publications reported that healthcare professionals believed that discussing eye donation would detract from the tranquil environment of a hospice and that donation requests could cause patients and their families physical and psychological harm [1,3]. However, service evaluation data reports that 86% (12/14) of doctors reported that conversations did not cause additional distress with 57% (8/14) reporting that the conversations about eye donation were perceived by patients and families as a positive outcome from the death [8].
Of note is that HCPs' perception that discussing eye donation would cause distress was not supported, in the retrieved records [4][5][6][7][8]. Three studies reported the attitudes, beliefs, or perceptions of patients [4][5][6], indicating that patients were willing to participate in discussions about the option of eye donation [5,6] but that patients were unaware of the option of eye donation or assumed that they were ineligible. Furthermore, participating patients were motivated to be eye donors and felt positive about the possibility of helping others [5,6].
A survey of inpatients [6] found that the majority of participants 73% (8/11) reported that they did not find it upsetting to discuss eye donation and that asking about donation enabled them to make an informed decision about donation. A further potentially important finding is that participants reported their preference to talk about eye donation while they were still well rather than when deteriorating [5].
Comments from nursing logs [7] after the introduction of an admission script that included questions about eye donation confirmed that patients (n = 121) and families were not aware of their eligibility to donate their eyes, but they were not concerned about the topic of eye donation being mentioned during admission. Nurses were positive about introducing the option of donation at admission [7].
Only one study mentioned cultural and religious beliefs as a barrier to eye donation [4], the study explored the views of 25 terminally ill cancer patients toward eye donation. The majority of patients [14/25 (56%)] were unwilling to donate their eyes based on their Buddhist beliefs that the body must remain untouched for eight hours after death to allow the spirit to depart and remain intact as the spirit should be able to see in the afterlife [4].
Publications that reported family/carer attitudes toward donation [2,8,12,13] found a lack of awareness of their dying family member's eligibility to be a potential eye donor. Findings indicated a range of beliefs including that donation was right, is a social duty to donate, and that it would be ''wasteful'' not to [2]. Family members' decision to decline eye donation was based on the prior stated wishes of the patient not to donate or the family's uncertainty about the patient's wishes [2,8].
Findings from across the retrieved dataset indicate that HCPs are a key barrier to the option of eye donation being raised [1,3,6,8] usually avoiding discussions about eye donation unless the issue is raised by the patient or the patient's family [1,3,6,12]. Although HCPs were cautious about discussing eye donation, patients [5,6] and carers [2,7,8] wanted to be informed and were not averse to holding discussions about eye donation. This points to a clear disconnect between the perceptions and beliefs of service providers and the perceptions of services users as reported in the existing literature.

Knowledge: Assets and Deficits
Five publications included HCPs reports of their knowledge about eye donation [1,3,[6][7][8]. In all studies HCPs reported knowledge deficits including not having sufficient knowledge about the process of eye donation [1] and lacking confidence to initiate eye donation discussions [3,[6][7][8]. However, training is not a guarantee that eye donation would be discussed [3] A study in the United Kingdom reported that 115/433 (27%) of HCPs had received some information, education, and training on eye donation, but 399/431 (93%) rarely or never raised the option of eye donation, with 357/433 (83%) of HCPs reporting that they did not know enough about eye donation in general terms to discuss it with patients and their families [3].
Furthermore, reviews of the literature including HCPs confirm the facilitative impact of education and training and that willingness to discuss donation is positively correlated to knowledge about the process of eye donation (referral and retrieval) and being aware of local policy and guidance [12,13].
Key knowledge deficits synthesized from the retrieved publications indicate that hospice and palliative care patients are generally unaware about eye donation and eligibility criteria [4][5][6]. For example, in two studies, patients thought they could transmit their cancer to recipients [4,5] or that their eyes would not be good enough for use in transplantation [4]; furthermore, next of kin are unaware that their dying family member with cancer could donate their eyes [2]. Retrieved evidence further indicates that not knowing the beliefs/wishes of the deceased regarding eye donation is a key barrier to increasing eye donation [2,8].

Discussion
Current literature in the donation and behavior change contexts continue to link attitudes toward a topic leading to a specific behavior taking place. For example, if people have a positive attitude toward donation generally, they will be willing to donate; however, authors report that attitudes alone are a poor indicator of behavior as the context within which an action takes place will cancel out favorable attitudes (Bracher et al., in press). 33 Early research reports no linear causal relationship between knowledge, values, attitudes, willingness, and action related to donation behaviours 34 with further modeling supporting the general finding that behavioral intention (or willingness) does not predict action. 35 Therefore, relying on changes in attitudes toward eye donation alone is not the route to increasing eye donation as the context within which discussions about eye donation need to take place is key.
This context within which discussions around eye donation need to take place is that of death. Apart from living donation, all donation options cannot proceed until someone has died; therefore, raising a topic that so profoundly signals impending death may be why HCPs are reluctant to raise the option of eye donation. A further consideration in the reluctance to raise the issue with family members is that death not only denies the next-of-kin of a significant relationship, but also robs them of many of their usual coping mechanisms, imposing a sequence of events that leave family members feeling dispossessed of physical and psychological equilibrium 36 ; therefore, HCPs may avoid what they perceive to be ''distressing topics'' due to concerns about the reactions of family members [7].
The retrieved evidence indicates that patients and family members are not averse to, nor distressed by, discussions around the option of eye donation, however, as with all end-of-life discussions timing is key. Evidence supports the benefits in ''introducing'' this issue at admission with this discussion being merely to assess donation status [7]. For example, a general discussion around being on the donor register and carrying a donor card. Adding eye donation to admission protocols would offer the opportunity to clarify potentially long-held plans to be a donor, which with the onset of a cancer diagnosis, would be limited to tissue and eye donation.
Furthermore, in raising this issue as part of ''the usual'' admission process, patients and family members are then able to discuss this option if they wish to and seek further information and guidance. As reported by the Organ Donation Taskforce 37 making donation ''usual'' as opposed to ''unusual'' is essential if donation rates are to increase. 37 However, early indications from a national study into the potential of eye donation from hospice and palliative care settings (EDiPPPP) is that both clinicians and the public are poorly informed about the need for eye donation, potential donor eligibility criteria, and the process of eye donation. It is essential that empirically informed interventions are developed that successfully raise public awareness and clinical confidence and competent in operationalizing the end-oflife option of eye donation.

Conclusion
This scoping review has provided an up-to-date appraisal of the current potential, perceptions, and practice underpinning offering the option of eye donation to dying patients and their family members in palliative and hospice care context.
Studies included in this review from one palliative care [6] and four hospice care [8][9][10][11] settings report that a total of 542 patients could potentially have donated their eyes. This equates to >1000 eyes from just these settings that could make a significant contribution to sight saving and sight restoring treatment and surgery.
The review outlines the key barriers to increasing eye donation from these settings include the reluctance of HCPs to raise this issue to avoid causing perceived distress to patients and their next of kin, and the evidenced lack of awareness of patients and family members about their own or their relatives donation options and eligibility. This review also indicates a lack of clinical guidance drawn from high-quality evidence proposing interventions that could inform HCPs' practice. The absence of this guidance is a barrier to change.

Limitations
Search strategy: in many articles, ''eye donation'' was subsumed under a wider term such as ''tissue donation'' or ''organ donation.'' This has implications for search strategies in future reviews focusing on eye donation, as relevant terms many not be directly visible to searches with a resulting risk of excluding articles that include eye donation as a subset of wider investigations. MeSH headings did not reliably include all relevant studies relating to the focus of this search. Those developing search strategies to underpin reviews may find it helpful to use a test set of familiar articles, as we have done here. None of the retrieved records included a diverse cultural participant group nor specifically looked at variables such as age, gender, and religious views, despite religious/cultural factors being evidenced as factors that influence organ and tissue donation decision making. [38][39][40]