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Original Clinical Science—General

Brain Death in Asia: Do Public Views Still Influence Organ Donation in the 21st Century?

Liu, Christopher W. MBBS, MMed1; Yeo, Charlene2; Lu Zhao, Boyu2; Lai, Clin K.Y. BA2; Thankavelautham, Suhitharan MBBS, MMed1; Ho, Vui Kian MBBS, MMed, FANZCA1; Liu, Jean C.J. BPsych, PhD2,3

Author Information
doi: 10.1097/TP.0000000000002562
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Abstract

INTRODUCTION

The determination of death is central to organ transplantation. Under the ‘dead-donor rule,’ cadaveric donors are required to be dead before organ procurement can occur.1 Accordingly, successful transplant programs require death to be clearly defined, with a definition agreed upon by the following: (1) healthcare providers, (2) the legal system, and (3) the public.

Amongst healthcare providers, a major shift occurred when the notion of ‘brain death’ was introduced. In the 1960s, a committee at Harvard Medical School discussed patients whose brains were irreversibly damaged, but who were kept alive through ventilators and resuscitative treatment.2 The committee subsequently published the first criteria of brain death, arguing that this diagnosis would prevent futile medical care and support organ procurement for transplants.3

Within 3 years of this report, Kansas and Finland became the first legal jurisdictions to recognize brain death.4 By the 1990s, nearly all Western countries had followed suit.5 Nonetheless, despite swift recognition within Western legal systems, brain death legislation proved to be more controversial in the East.5 Asian countries adopted brain death into their legal lexicon at a later stage, with Singapore, Taiwan, and Sri Lanka—the first Asian courts to do so—enacting legislation nearly 2 decades after their Western counterparts (in 1987).6 Further, although most Asian countries now recognize brain death,6 this has come with more stringent guidelines and a lower rate of brain death certifications (relative to Western countries).5,7

Public Views of Brain Death Within Asia

Given the restraint of Asian legal systems, a corollary question is whether East-West differences also characterize public views. Arguing for a difference, many commentators have recounted the heated public responses toward brain death laws in Asia. This was particularly true for Japan, where the acceptability of brain death was fiercely debated for 30 years until it was recognized (through the Law on Organ Transplantation in 1997).8-11 Even in Singapore—one of the first Asian countries to enact legislation—members of the public have questioned the legitimacy of brain death in media outlets.12,13

Beyond historical accounts, few surveys have systematically documented layperson views of brain death within an Asian country.5 In one study published in 2010, Japanese respondents were asked whether they perceived brain death to be a reasonable standard for human death.14 A mere 43% agreed, as compared to 60%–71% of respondents from Western countries (Germany, United States, France, and Britain).14 Similar rates were reported in a 2013 survey from China (34% acceptance of brain death),15 and a 2003 survey from South Korea (51.8% positive toward brain death).16 Finally, in a 2006 survey involving Japanese university students, only half the respondents were familiar with brain death (51.5%), and just over a third (38.8%) accepted the notion.17

Although these survey results converge with the strong reactions previously expressed toward brain death legislation, it remains unclear: (1) what exactly the Asian public understands brain death to entail, (2) how views toward brain death are compared with those of cardiopulmonary death, (3) and the extent to which brain death perception may be related to the low rate of deceased organ donation observed amongst Asians.8,18,19 Further, extant research largely dates back to a decade ago, and may not generalize to the present day.14-17 Recent surveys suggest that despite a slow start, the majority of Chinese medical providers and policy makers now understand brain death20 and consider it an acceptable standard of death.20,21 It is thus possible that with time, brain death may have likewise been normalized within the general public.

To address this gap, we conducted a nationwide survey of views toward brain death in Singapore. As an Asian country, Singapore’s key indicators matches those of Western countries with developed economies (language of instruction: English, gross domestic product per capita: USD $51 880,22 percent of adults with postsecondary qualifications: 54.2,23 and life expectancy at birth: 82.9 y23). However, its ethnic and religious composition matches those of the region (44% Buddhists/Taoists, 15% Muslims, and 5% Hindus),24 and provides a window into Asian views even after educational and economic indices have been matched. Finally, Singapore has had 30 years of history with brain death legislation, and serves as a natural experiment to explore whether legal provisions have normalized brain death within an Asian country.

MATERIALS AND METHODS

Study Design and Population

A cross-sectional survey was conducted door-to-door with adults who qualify as organ donors under Singapore’s Human Organ Transplant Act.25 Based on this requirement, the study population comprised Singapore citizens and permanent residents aged ≥ 21-years old. The study was approved by the National University of Singapore’s Institutional Review Board (IRB A-16–131), and was preregistered on ClinicalTrials.gov (HSS-1502-P02-01). All participants gave verbal consent, and surveys were conducted between September 2016 and July 2017.

Survey Administration

To obtain a representative sample, households were identified using cluster-sampling followed by simple random sampling. As Singapore is organized in districts served by community centers, 6 centers were first selected at random and a cluster was defined as all residential dwellings within 1 km of the center. Within each cluster, 4 to 5 residential postal codes were selected at random, ensuring that the distribution of house types approximated that of the nation (in every 100 dwellings: 80 public apartments, 14 private apartments, and 6 landed properties). For each postal code, trained interviewers then systematically knocked on doors during weekday evenings (6 to 9 pm) or weekends (9 am to 6 pm) each week during the data collection period. For apartment blocks, this involved approaching each household from either the lowest to the top floor, or from the top to the lowest floor. If a household could not be contacted, a second attempt was made 1 to 3 hours later.

When households were reached, random person selection was accomplished by identifying the person whose birthday was most recent. Interviewers then described the study, disclosing (as an IRB requirement) that questions would involve the topic of death. Upon providing verbal consent, participants completed the questionnaire booklet on their own unless they requested for assistance. (Being mindful of cultural sensitivity, interviewers did not ask participants the questions in case they were uncomfortable discussing death.) All participants were then reimbursed SGD $10 for their time.

Questionnaire Development and Testing

Questions on brain death were part of a larger 30-minutes survey exploring organ donation views in Singapore (https://osf.io/73x9j). The full survey booklet contained 42 questions derived from previous large-scale national surveys,26-28 and pertained to the following: (1) opt-out versus opt-in policies; (2) brain death and organ donation; (3) other death-related procedures; (4) knowledge of Singapore’s organ donation laws; and (5) demographics. The questions reported in this article focused on death itself (rather than the postdeath stage), and were included in the second section.

Understanding of Brain Death

To investigate participants’ understanding of brain death, the first item was drawn from a similar survey administered to the Canadian public.27 Respondents were asked to select whether brain death meant the patient was (1) dead, (2) in a coma with no realistic chance of survival, (3) in a coma with a small chance of survival, (4) in a coma with a good chance of survival, or (5) in a coma with a good chance of recovery; participants could also indicate if (6) they did not know.

Brain Versus Cardiac Death

Participants were also asked to compare brain and cardiac death directly. Using 5-point scales, participants rated (1) the extent to which they thought cardiac death was a better indicator of death than brain death (1 = “Strongly disagree,” 5 = “Strongly agree”); (2) whether they would be more willing to donate their organs after brain than cardiac death (1 = “More willing to donate upon cardiac death,” 5 = “More willing to donate under brain death”); and (3) whether they would be more willing to donate a family member’s organs after brain versus cardiac death (1 = “More willing to donate upon cardiac death,” 5 =“More willing to donate under brain death”). In each case, a rating of 3 indicated neutrality—that is, being impartial to cardiac and brain death as an indicator of death or the context of organ donation.

Impact on Organ Donation

Finally, we investigated how views toward death might impact reception toward organ donation after brain death.26,27 Again using a 5-point scale (anchored on one end with 1 = “Strongly disagree” and 5 = “Strongly agree”), participants rated the extent to which they feared that they may not be fully dead before their organs are used for donation.26,29 They also rated the extent to which fear of not being fully dead concerned them regarding donation of their family member’s organs (1 = “Strongly disagree,”, 5 = “Strongly agree”).

Survey Translation

The full survey booklet was made available in the 4 official languages of Singapore: English, Malay, Tamil, and Mandarin. As the original questions were in English, the booklet was translated into the remaining 3 languages by native-speaking language teachers (with 2 translators per language). For verification, the questions were then back-translated into English by a third translator. Across all languages, survey items were written at a 7th grade reading level and were pilot-tested for clarity.

Statistical Analysis

As the primary analysis, survey responses were summarized with counts (%) and medians (with interquartile ranges [IQR]). Where comparisons were made with other national surveys, we ran 2-sample tests for equality of proportions (with continuity corrections). Two follow-up exploratory analyses were conducted as described below: a classification tree to predict brain death understanding from demographic variables, and a path model to explore the relation between the surveyed aspects of brain death.

For all statistical tests, Type 1 Decision Wise Error Rate was controlled at α = 0.05. Based on power calculations, a sample size of 600 was required to obtain a 4% margin of error for estimates of proportions (given a conservative proportion of 0.5).30 Accordingly, as the stop rule, data collection was scheduled to cease when 600 respondents had been recruited or when staffing contracts concluded (whichever provided a larger sample size). All analyses were performed in SPSS 24 and R 3.4.0.

RESULTS

Response Rate

Of the 1031 households who completed the study briefing, 622 (60.3%) provided verbal consent and participated in the study, and all but 23 (96.3%) returned nonempty survey forms to the interviewers (Figure 1). Six participants were removed from statistical analyses because their self-reported age on the survey (<21 y) did not qualify them for the study (despite having reported an older age to the interviewers).

FIGURE 1.
FIGURE 1.:
Flow diagram of survey participation.

The final sample of 593 respondents (Table) was comparable to the Singapore population in gender, age, ethnicity, and religion (≤5% difference), but had a greater representation of households from public housing (92% vs 79%);31 participants were also more likely to have received tertiary education (58.7% vs 44%).31

TABLE.
TABLE.:
Baseline characteristics of survey respondents

Understanding of Brain Death

As shown in Figure 2, most participants (65.5%, 95% CI, 61.7%–69.3%) perceived brain death to have bleak outcomes (a coma with no realistic or small chance of survival). However, only 14% (95% CI, 11.2%–16.8%) equated brain death with death—a proportion significantly lower than that observed in national surveys from Canada (29%; χ2[1, N = 2098] = 50.43, P < 0.001)27 and from the United States (40%; χ2[1, N = 1944] = 122.80, P < 0.001).32

FIGURE 2.
FIGURE 2.:
Participants’ understanding of brain death. Shaded bars represent the percentage of participants who agreed with each view of brain death, and vertical lines represent 95% confidence intervals. As a comparison, the unshaded bars depict the percentage of participants who defined brain death as ‘death’ in previous North American surveys.

Given the low recognition of brain death, we used a tree-based model to identify demographic variables predictive of brain death understanding. Using recursive partitioning (from the R package “rpart”),33 we generated a classification tree with the following predictors: gender, age, ethnicity, religion, country of birth, marital status, education, house type, whether the person had an immediate family member who was not of Asian ethnicity, and whether the person had lived overseas. This classification tree allowed us to assess multiple demographic variables simultaneously, and allowed for complex relationships between predictors to be explored.34 However, when cross-validation was applied to determine the size and shape of the tree, we found no stable variables that systematically predicted whether participants characterized brain death as death. (Our conclusions did not change when we repeated the analyses using a logistic regression model.)

Comparing Brain and Cardiac Death

When participants were asked to rate, on a 5-point scale, the extent to which they perceived that “cardiac death (was) a better indicator of true death than brain death,” their median rating was 4 (IQR: 3 to 5)—general agreement with the statement. This corresponded to half the participants judging cardiac death to be a better yardstick of death than brain death (95% CI, 46.1%–54.3%; Figure 3).

FIGURE 3.
FIGURE 3.:
Pie charts of how participants perceived brain vs cardiac death. Participants indicated (from left to right): which of the 2 they considered a better indicator of death (N = 573, did not answer = 20); when they were more willing to donate their own organs (N = 558; did not answer = 35); and when they were more willing to donate a family member’s organs (N = 550; did not answer = 43).

Despite leaning toward cardiac death as an indicator, participants gave a median rating of 3 (IQR: 2 to 3) when asked the extent to which they would be willing to donate either their own or a family member’s organs under cardiac versus brain death. Nonetheless, 1 in 3 participants indicated greater willingness to donate under cardiac than brain death (95% CI for own organs: 31.6%–39.6%; 95% CI for family member’s organs: 29.4%–37.2%; Figure 3).

Impact on Organ Donation

Thus far, our findings suggest that cross-cultural differences in the understanding of death may pose a challenge for organ donation. In line with this view, we found that when participants considered donation in the context of brain death, 31.2% (95% CI, 27.5%–34.9%) expressed a fear of not being fully dead before their organs are used for donation (Figure 4). This proportion was higher than that observed in previous large-scale surveys involving Swedish adults26 (range of 10% to 22%) and youths35 (17%; χ2[1, N = 2040] = 50.60, P < 0.001). Notably, our observed levels of fear were also higher than that of the Denmark public (12.7%; χ2[1, N = 1788] = 87.26, P < 0.001)—despite Denmark’s late introduction of brain death laws historically.29

FIGURE 4.
FIGURE 4.:
Participants’ fear of not being fully dead should organs be transplanted upon brain death. Respondents indicated whether they shared this fear (‘agreed’) regarding organ donation from: a family member (top bar) or themselves (second bar). As a comparison, the bottom 3 bars indicate responses for the self in previous European surveys.

When participants were asked to consider donation of a family member’s organs upon brain death, 35.7% (95% CI, 31.8%–39.6%) of participants likewise expressed a fear that their family member may not be fully dead upon donation. Thus, their anxiety toward the diagnosis of death extended to both themselves and to family members.

Toward a Model of Brain Death Acceptance

As exploratory analyses, we computed Spearman’s correlations for each pair of ordinal variables pertaining to brain death (see the sections Comparing Brain and Cardiac Death, Impact on Organ Donation, and the current section Toward a Model of Brain Death Acceptance). As shown in Figure 5, the perception of cardiac death as a better indicator of death (‘perception of death’) was associated with (1) greater fear of not being dead during organ donation (‘fear of not being dead’), and (2) decreased willingness to donate after brain death (‘willingness to donate’). In turn, fear of not being dead was inversely associated with willingness to donate.

FIGURE 5.
FIGURE 5.:
Heat map showing Spearman’s correlations between brain death variables.

As this pattern of associations met the preconditions for mediation, we formally assessed whether the relationship between death perception and willingness to donate was mediated by fear. This was tested using the R package ‘lavaan,’36 using 5000 samples with replacement. Indirect effects were deemed significant if the confidence intervals for the estimates did not include zero.

As shown in Figure 6, respondents’ fear of not being dead upon organ donation was a partial mediator between perception of death and willingness to donate. Even with fear accounted for, the direct path between perception and willingness to donate remained statistically significant. Thus, respondents’ perception of brain death had both direct and indirect effects on their willingness to donate under brain death.

FIGURE 6.
FIGURE 6.:
Standardized regression coefficients for the relation between perception of death and willingness to donate, as partially mediated by the fear of not being dead upon organ donation. Confidence intervals are shown in brackets.

DISCUSSION

In this study, we conducted a nation-wide survey to investigate public views of brain death within Asia. This was assessed in a ‘best-case’ scenario—in a country where brain death legislation has been in place for 3 decades, and where socio-economic metrics match those of major Western countries.22,23 If these factors were sufficient to influence brain death acceptance, we would expect participants to report views similar to those in North America or Europe. Instead, we found a high level of resistance toward the brain death diagnosis: first, when respondents defined brain death, only 14% recognized it as death—a proportion lower than that observed in previous North American surveys.27,32 Second, respondents were more likely to perceive brain death as a poorer indicator than cardiac death. Third, this view predicted concerns regarding deceased organ donation, with 1 in 3 respondents fearing that they may not be dead if their organs were transplanted upon brain death—again a proportion higher than that observed in previous European surveys.26,29,35 Finally, both perception and fears predicted a decreased willingness to donate organs after brain death.

Taken together, our results underscore the extent to which the lay public views brain death warily in Asia. Indeed, cultural influences are so pervasive that we found no demographic variable predicting the recognition of brain death as ‘death.’ By contrast, other East-West differences in organ donation attitudes (eg, views on treatment of the dead, views of organ donation, trust in doctors) have been found to vary across ethnicity, religion, and age—even within an Asian population.19,37 Instead, low acceptance of brain death appears to be more uniform across subgroups, and is seemingly resistant to the passing of time or of legislation.

Our survey mirrors historical accounts, where brain death legislation had a slow uptake across Asia.5 Although each country has had idiosyncratic reasons for strong public reactions to these laws (eg, in Japan, a controversial heart transplantation was performed in 196838), commentators have speculated that there are broader philosophical and religious influences in the region.5 These, they argue, have led Asians to value a holistic mind-body perspective, the preservation of life, and the desire for a natural course to death.5,9 Against this backdrop, they further argue, the brain death diagnosis upholds the incompatible notion that personhood resides within the brain.5,11 Thus, if care is withdrawn or organs transplanted upon brain death, this could be considered within Asia as a deliberate act of taking life away.10 Our findings add to the literature by providing empirical support for these claims, since participants reported high levels of fear that a person may not be truly dead during brain death, and were more comfortable with cardiopulmonary death (when all bodily functions have ceased).

Policy Implications

Given this understanding, our findings may partly explain why deceased organ donation has been low amongst Asians—including those residing outside Asia (eg, Australia)—despite attempts to reverse this trend.8,18,19 While previous cross-cultural surveys explained the low rates in terms of a greater belief that the body should be buried whole,37,39,40 a poorer understanding of organ donation,19,39,40 and poorer trust in doctors,37,39,40 our study emphasizes how concerns about deceased organ donation start at the point of determining what ‘deceased’ means. Without agreement between the public, healthcare providers, and the legal system on this definition, Western strategies to boost organ donation—such as moving from an ‘opt-in’ to an ‘opt-out’ system41—will likely be of limited value (since these assume a common understanding between stakeholders).

Moving forward, transplant programs targeting Asians need to address how death is determined. This target is likely a difficult one as several religious leaders have already expressed support for brain death (eg, the Islamic Fiqh Academy and the Islamic Organization of Medical Sciences).42 Nonetheless, a recent study found a small effect of education in a Korean intensive care unit: when families of patients were briefed extensively on brain death, 1 in 4 participants who had been unwilling to donate their family members’ organs subsequently changed their minds.43

Beyond education, one way of emphasizing the holistic nature of a person may be to avoid distinguishing “brain death” and “cardiac death.”44,45 These terms suggest the death of an organ, and may be particularly unhelpful within an Asian context. In contrast, there have been several attempts to unify the definition of death45,46—for example, by defining death as “a time when there is permanent loss of capacity for consciousness and loss of all brainstem functions… (that) may result from permanent cessation of circulation or catastrophic brain injury.”45 If patients are referred to as ‘dead’ rather than ‘brain dead,’ this could help family members accept the diagnosis as true death. Nonetheless, we urge further research and debate, lest such a strategy—though well-intentioned—is misconstrued as ethical gerrymandering.

Although we have discussed public views on brain death, we emphasize that this is not the sole factor responsible for low organ donation rates in Asia. Indeed, countries such as Spain and Croatia have found that successful organ donation programs require a multipronged approach.47-50 This includes appointing well-trained transplant coordinators at every hospital, donor identification strategies, protocols to minimize family refusals, and public education.47-50 Complementing these well-established factors, we suggest that Asia’s transplant programs also need to consider cultural views toward brain death.

Study Limitations

In drawing policy suggestions, we note several limitations of our study. First, as death is a taboo topic within Asia,51-53 our surveyors could not record participants’ responses directly (and instead allowed participants to complete the questionnaire themselves). Second, as a multicultural country, our questionnaire was translated into the 4 major languages of Singapore. Although most participants completed the survey in English (85%), and though translation took place according to best practices,54,55 the possibility remains that there were nuanced differences in meaning for those who read the non-English versions (as is true of all translated documents).

Finally, several important questions remain unanswered. In terms of methods, we have reported an association between acceptance of brain death and one’s willingness to donate. Although this is consistent with the notion that resistance toward brain death could contribute to low organ donation rates in Asia, our correlational findings do not establish this causality, nor did we measure actual donation behaviors. In terms of policy-making, it remains unclear: (1) what the exact basis is for rejection of brain death (eg, a matter of knowledge, or an inability to accept brain death for reasons other than knowledge); (2) the cultural elements at play (eg, individualism vs collectivism, attitudes toward science and medicine); (3) at which stage of organ donation brain death acceptance might have a role (eg, signing a donor card, family refusal); and (4) what interventions can best address brain death acceptance in Asia. Moving forward, we encourage further research that will allow policies to be optimized for organ donation.

CONCLUSION

In conclusion, we report in this study pervasive East-West differences in the acceptance of brain death. Although the gap has narrowed with both the law and healthcare practitioners, reservation toward brain death persists amongst the general public. This continues to hamper deceased organ donation, and novel and multidisciplinary approaches are needed to shift public opinion. In short, the pursuit of life in Asia (through organ donation) requires further exploration of death.

ACKNOWLEDGMENTS

The authors gratefully acknowledge Chow Kit Ying, Sean Nicholas, Hans Toby Limanto, Sophie Ang, Dinh Hai Bao Lien, Claris Nghai, Pei Jia Ying, and Nasir Ruslan for their assistance in the preparation of surveys, data collection, and data entry.

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© 2019 The Author(s). Transplantation Direct. Published by Wolters Kluwer Health, Inc.