Death determination by neurologic criteria (DNC), or “brain death” as it is commonly known by the general public, is based on the cessation of brain function. Physicians make this determination following a series of medical tests to ensure specific criteria are met.1 While members of the health care team are familiar with DNC, prior studies have confirmed that the general public often struggle to grasp the medical concept of death and death determination elements.2,3,4,5,6,7,8,9,10,11,12,13 Exacerbating this confusion is the media’s frequent misuse of language describing various aspects of death and dying.6,8 Notably, the media typically confuse the distinctions between brain death, coma, and persistent vegetative state.5,6,12,13,14,15 Little empirical evidence exists that examines the family perspectives on death and DNC, particularly in the context of confronting the imminent loss of a loved one.

Within the intensive care unit (ICU), family is defined by the patient, or in some cases, by the patient’s surrogate(s). As such, family members (FMs) may be related or unrelated to the patient but are generally individuals who provide emotional support and with whom the patient has a significant relationship.16 Understandably, when FMs must confront the reality of a loved one dying in an ICU with a DNC, the experience may be fraught with confusion. For some FMs, the determination of death is at odds with what they observe before them.4,17 After DNC, despite the permanent cessation of brain function, the body of their brain-dead relative remains warm, and their technologically supported body retains many essential biological functions, including a heartbeat, systemic circulation, digestion, and excretion.3 The uncertainty and tremendous stress experienced by FMs at this time can negatively impact their decision-making processes and limit their capacity for rational thinking.18,19,20,21 It is of utmost importance to understand FMs’ perspectives on DNC to support them not only during their time in the ICU but also in the weeks following discharge as they grieve the loss of their loved one and attempt to make sense of what has happened. When FMs have unanswered questions or difficulty accepting a death, it is linked with complicated bereavement outcomes.18,19,22,23

At present, little empirical data exist on how to address when family misunderstandings about brain death and death determination do not align with the medical diagnosis.8,19 The objective of this study was to describe FMs’ understanding of brain death and the process of determining death in the context of organ donation within Canadian ICUs. Doing so can inform clinical practice as well as the development of bedside tools to improve FMs’ comprehension of DNC and aid them while making difficult decisions related to organ and tissue donation. Such tools are in line with the provision of patient and family-centred care, an approach to health care delivery that is respectful of and responsive to individual patients’ and families’ needs and values.16

Methods

Design and setting

This study was part of a larger Canadian-based qualitative study involving in-depth interviews with FMs asked to consider organ donation following DNC. The present study focused specifically on FMs (n = 179) of DNC patients. An earlier publication outlined the larger study protocol.24 All study recruitment, data collection, and data analysis occurred after approval from multiple Canadian institutions’ Research Ethics Boards (see Electronic Supplementary Material [ESM] eAppendix 1) and are reported according to the consolidated criteria for reporting qualitative research guidelines (see ESM eAppendix 2).

Recruitment

All Canadian provinces with an organ donation organization (ODO) participated (n = 9). Family members were eligible for the study two months to three years after the death (DNC and death determination by circulatory criteria [DCC]) of their loved one, irrespective of whether or not they agreed to proceed with organ donation. Each ODO compiled a database of eligible FMs, including their names, telephone numbers, address, sex, relationships to the patient and donation decision, and the manner of death determination (neurologic or circulatory criteria) (n = 1,500). A total of 236 FM names were excluded because of language barriers and/or a lack of family contact information. Organ donation organization staff contacted FMs by mail to inform them of the study. Approximately two weeks later, ODO staff telephoned these individuals to explain the purpose of the study, and to request their permission to be contacted by research staff. A total of 338 FMs agreed to be contacted by the research team. Next, research staff contacted the FMs to explain the study, and to schedule a telephone interview with consenting individuals. Of the 338 FMs who agreed to be contacted, 265 agreed to proceed with an interview. Two ODOs contacted FMs in a different manner. In Ontario, letters were not sent; instead, ODO staff contacted FMs by telephone within six months to one year after the death of a loved one. In Quebec, letters were sent to eligible FMs informing them of the study but also requesting a mail reply if they were interested in participating; only interested FMs (based on their mailed reply) were then contacted by the ODO staff.

Data collection

Informed by an earlier study of FM experiences in Ontario, we developed a semistructured interview guide to explore family interactions with health care teams within the ICU (see ESM eAppendix 3).21 An interdisciplinary team of investigators with experience in critical care, palliative care, organ donation, medical education, and sociological and qualitative research methods provided feedback to refine the interview guide. Next, we solicited feedback on the guide from a committee of FMs, members of the Canadian Critical Care Trials Group and organ donation leaders representing every ODO in Canada, and revised it based on their feedback (see ESM eAppendix 3 for guide). Members of the research team with prior interview training and experience conducted the telephone interviews using the semistructured interview guide. While the guide provided a predetermined line of inquiry, it was flexible enough to evolve as data collection unfolded, permitting the exploration of emerging themes. If requested by participants, multiple FMs were interviewed together, for example a mother and father. All interviews were audio-recorded and occurred between July 2018 and June 2020. The interviews lasted anywhere from 45 to 90 min.

Data analysis

All interviews were audio-recorded, transcribed verbatim, and uploaded into ATLAS.ti (Scientific Software Development GmbH, Berlin, Germany), a qualitative data analysis software, to facilitate data management and analysis.25 The method of analysis was a modified grounded theory approach. The analysis was performed by five members of the research team (A. S., S. S., A. L., B. V. W., and S. V.) who participated in regular coding meetings to develop the codebook (see ESM eAppendix 4). The codebook included both inductive and deductive codes. All five analysis team members coded the same transcript separately, then met to discuss their codes, refine code definitions, and resolve any coding disagreements.26 This process was repeated until the level of coder agreement, measured using Krippendorff alpha, reached a value of 0.858%;27 thereafter, independent coding began. Later, codes were organized into themes relevant to the study objectives. Analysis procedures also included using the Atlas.ti query tool to interrogate the data set using Boolean operators for the codes of interest, including brain death, family conflict/brain death, and death determination. The resulting reports were then coded to define subcodes, which permitted elaboration on the themes. The recommendations from FMs were developed by assessing the qualitative themes for quotes, whereby FMs explained how certain events helped or hindered their understanding of DNC. These quotes were aggregated and written into short, action-oriented prose.28

Results

Overall, 265 telephone interviews were conducted; in six interviews, two FMs participated together. Of the 271 FMs interviewed, 179 were interviewed about a patient who underwent DNC. The other 92 FMs were interviewed about cases of DCC and were not included in this analysis.

Table 1 describes the 179 DNC study participants in terms of their province, sex, and relationship to the 174 DNC patients. Most patients in the study were male (N = 103) aged 19–30 yr followed closely by those in the 51–60 yr and 61–70 yr age ranges. Table 2 illustrates the six qualitative themes with a data display allowing for additional quotes to depict each theme.

Table 1 Characteristics of 179 participating family members of DNC patients
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Table 2 Qualitative themes with illustrative quotations
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State of mind

Family members described their state of mind impacting all their recollections of brain death and death determination. Many explained that this state rendered them unable to “hear” and/or retain the information that health care professionals (HCPs) provided. Family members explained being unable to comprehend information about their loved one and needed to have things repeated many times to absorb the details:

It was really hard to understand because two doctors came in and told whoever was in the room with us, “Unfortunately we weren’t able to save him and it didn’t look like there was any brain activity”… something along those lines. I was not able to comprehend what they were saying. All I remembered at that time was the word “unfortunately.” “Unfortunately,” just gave me what I needed to know. I couldn’t even hear them properly because I went into this state where I was thinking I wasn’t hearing things right.

Communication

Given FMs’ state of mind, and the complex nature of brain death, families recalled needing HCPs to take time and present information in a clear and concise manner. This entailed detailed descriptions and/or having information repeated:

The doctors were trying to explain it to me and I remember them saying that they had to go up and do testing that takes about one hour. A piece of me thought, maybe there’s a chance that there’s brain activity? But they were trying to explain to me that there was no brain activity but they had to do these tests to have 100% proof. They had to get very descriptive with me, which is unfortunate because it’s a piece that’s been the hardest for me to process about his death. They described the size of the bullet and how it went into his head and it didn’t exit … some people die immediately from a gunshot to the head but his bullet was so small that it bounced around it didn’t have enough power to escape the skull. The bullet bounced inside and destroyed his brain. They had to get that detailed with me because I couldn’t comprehend what they were saying.

Family members described not understanding the distinction between coma and brain death:

The neurologist briefly explained to me what happened because [Name 1] was in a coma at that point. I knew he was in a coma and he had been unconscious but I really didn’t know what it meant. At one point I thought, “Oh he could wake up in five minutes or in an hour.” I was fully expecting him to wake up and be fine. There was a point where I sort of went, “Okay I know he was without oxygen” … I thought he was going to wake up or he might have some deficits because I understood he didn’t have enough oxygen for a certain period of time, but I didn’t appreciate the gravity of the situation at that point because I didn’t have that information.

Many FMs recounted the importance of multimodal communication such as written notes and/or diagrams as well as having been shown radiographic images, when appropriate:

Nothing was written down, so I have no written record of what was done. I was told, verbally, but I don’t remember. I remember them saying we had done the tests but I’m not sure what that included.

Brain death as counterintuitive

Family members explained that the diagnosis of brain death seemed implausible or contradictory to how their loved one looked. In particular, FMs experienced difficulties understanding that their loved one could be brain dead given the fact they appeared as though they were sleeping:

That was the hard part, when you would go in to see him and he looked really good, because, of course he was on life support so the machines were doing the work, but he looked really good. It was eerie that way. You feel a little bit guilty leaving them there knowing they’re still there. His hand is warm, his chest is rising, his heart is beating. And, they were keeping his eyes lubricated. So, every once in a while, you would see, saline come out of his eye. It was like, oh my God, but it’s your heart and your mind playing tricks on you a little bit. It’s still not an easy thing to process, because your heart is breaking.

Preparing for the death determination by neurologic criteria clinical assessment

Family members explained their preparedness, or lack of preparedness, on a continuum. At one end, FMs recounted not being told the DNC testing was going to happen. While some FMs felt they were not adequately prepared, others did feel ready for the assessment. Many FMs expressed frustration, and even suspicion, when the DNC clinical assessment was delayed, or needed to be repeated, without explanations from HCPs. The first quote is a description of a FMs reaction when they are not adequately (or not at all) prepared for the DNC clinical assessment:

The one doctor said that he would speak to the family, so it was myself, my husband, my son-in-law and his parents who went into a room and they told us that they had declared her brain dead, and that there wasn’t anything they could do for her and that was it. I guess that was their protocol and they made the decision so that the family didn’t have to, and then they were going to send somebody in to talk about donating her organs. We didn’t realize that they would have called her time of death without talking to us first. I’d never been through anything like that before ... we had no idea what to expect. It was shocking.

Family members who were not provided sufficient details of DNC (e.g., various processes including timing of death) reported feeling additional confusion and anxiety:

They kept saying to me that they had to let my mom, and I don’t know maybe it’s because of what medical issue was going on with her, but they said they had to let her die. There was a lot of uncertainty for us. I remember them telling us that they needed her to experience brain death and she wasn’t there yet. The doctor would say, “Okay, we’re going to check to see if she’s dead” It was a weird situation because I knew they were trying to keep her alive for the donation but then also she had to experience brain death. I think that’s what was going on. I remember them checking and then telling us, “She’s actually still not dead yet so we’re going to wait like a few more hours.” And then having to do it again. I wasn’t given any kind of a clear time.

Clinicians who provided clear and straightforward explanations that met the FM’s needs resulted in gratitude and acceptance:

The doctor explained everything. I really didn’t have any questions because he explained it all so well and if I did have questions, he answered them, and I trusted his answers. I know I asked, “How do you know exactly he’s brain dead,” you know those things? And so, we had a real in-depth conversation and he explained how the brain functions and in 24 hours you can tell if its healing or what have you, and these are the tests we do. He made sure that we knew there was no chance of recovery. We laid our trust on the doctor, and we felt comfortable with that.

When delays and/or the need for additional testing was not clearly explained, some FMs became suspicious of the medical team’s motives:

It was always made to sound like it was on our schedule and the doctors needed to confirm the death. At one point they said, “Oh, we think there was some movement in some baby toe or something, so we have to redo some tests.” And I went, “Come on! Really?” I think they were stalling for time and I don’t have a problem with that if they had been totally upfront. There was no way [Name 1] was going to be alive again, so let’s get on with this.

The death determination by neurologic criteria clinical assessment

Family members articulated the importance of being invited to be present and witness the DNC clinical assessment, specifically the apnea test. The first two quotes are illustrative of how beneficial it was to be present for the apnea test:

… and then the doctor said, well we’ll do a third test, I told him that I need to know, because you always hear about these miracles, you know, that people can just come out of this. Do you know what I mean? I told him I can’t make a decision until I know for sure, so they said would do a third test. I was there and they took him off the respirator and if he breathed on his own, then there would be brain function, that’s what it was. Yeah, and he didn’t, so then I knew for sure. It was so helpful.

They did the test where they blew the CO2 into his vent to see if he triggered a breath. When he failed that the doctor was nice enough to do another EEG to confirm it, but he basically said that he had to pronounce him dead at that point. It was kind of conclusive that he had failed that test and that was the end of the road. When he said, “I have to pronounce,” it was shocking to us that he used those words. So, that’s when I said, “oh, I got it.” They spent a significant amount of time explaining things to us and I’m not talking two minutes here or two minutes there, I had more than a couple of hours of full discussions, and this as I understand is the neurosurgeon and obviously, he is a busy guy.

Family members wanted the option to be invited to attend the DNC clinical assessment and when they felt as though they were not welcome to be present, they reported more negative bereavement outcomes:

They just kind of came in, shooed me out, did some tests and then let me go back in. And then I waited and waited and waited, and then they came and said “Okay, we’re done.” It was really hard on me.

Time of death

The legal time of death appeared to be confusing for many families. Family members experienced guilt if they felt their loved one was declared dead in their absence:

I wasn’t in the room at the time they issued the death certificate, and I struggled with that. When had they declared the time of death? It would have been very late and the donation operation wasn’t until, 11:00 or something on the 6th? It was a night time surgery, so I wasn’t there and this idea of him passing without me by his side is really difficult.

Families struggled with the distinction between when the person died and when the body died:

Mother: She wasn’t brain dead ‘til 5:00 o’clock. Like her body, I guess you’d say was dead, but her brain wasn’t dead so for them to pronounce her dead was at 5:00 o’clock on the 5th.

Father: When the doctor called us at 11:00 o’clock, they said that she was already unconscious, that she was nonrespondent but she wasn’t dead or brain dead.

Table 3 illustrates the six broad and overlapping themes that emerged from the FM data, phrased in terms of practice-based recommendations to improve FM understanding of brain death and death determination in the context of organ donation.

Table 3 Family generated recommendations and changes in HCP practice
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Discussion

We conducted a large, high-quality qualitative cohort study of FMs experiences of understanding brain death. We described FMs’ understanding of brain death and death determination in the context of organ donation within Canadian ICUs and have provided family-generated recommendations to improve understanding and acceptance. Family members’ understanding of brain death and death determination represented a journey that was reported as sequential meetings with HCPs, most notably physicians. Family members in our study indicated that the process of death determination, specifically bedside clinical assessment including observing the apnea test, was critical for providing concrete understanding and often closure. Nevertheless, some families felt they were not welcome to attend clinical assessments, including the apnea test, and these FMs were more distrusting of the medical team and reported more negative bereavement outcomes.

Family members described a state of intense grief and exhaustion, which impaired their capacity to think rationally or objectively, consistent with previous studies.17,20,21,22,23 In their state of mind, FMs must endure an additional psychological burden as they struggle to comprehend brain death, a construct that research has shown to not be well understood by members of the general public.3,4,5,6,7,8,9,10,11,12,13,14 Many FMs explained their state of mind often rendered them unable to “hear” and/or retain the information that HCPs provided. FMs explained being unable to comprehend information about their loved one and needed to have things repeated many times to absorb the details.

Our data, as others’,8,9,11,12,13,14,15,19 reveal that many FMs struggle with the difference between brain death and coma, and some continue to struggle with this differentiation years after the death of their loved one. Despite several decades of research on this topic, many FMs, and the public continue to be confused about the differences between brain death and other neurologic disorders such as comas or persistent vegetative state.8,11,19,29,30,31,32 We have found that the timing and frequency of conversations with families are important for their comprehension. Families need to be informed early in the death determination process, and need to have information repeated several times to understand. Moreover, multimodal communication strategies (e.g., notes, diagrams, images) are critical for FM reference thereby helping to ensure they do not have unanswered questions about the process. A growing body of research finds that bereaved FMs who lack understanding of brain death are at a higher risk of developing symptoms of post ICU syndrome, such as anxiety, depression, and post-traumatic stress.18,19,23,33

The counterintuitive nature of brain death served to contribute to FMs’ confusion. Indeed, appearances can be deceiving as FMs try to reconcile the ambiguity of the dead body’s appearance. We, as others have shown,4,34 found that conflicting sensory information including touch (feels warm) and visuals (see them breathing), challenges the acceptance of DNC. Accepting DNC for someone who appears to be still breathing and whose heart is still beating, albeit with support of ventilators or other devices, seems to violate a basic understanding of what constitutes life.35 Similar to Tawil and colleagues study findings,34 FMs confirmed that when they were able to witness the DNC clinical assessment, they were able to overcome any lingering conflict and move towards acceptance and closure.

Less reported in the literature are depictions of FMs who witnessed death determination testing, specifically the apnea test. FMs were clear that being present for the apnea test was beneficial on three important levels: 1) they clearly understood that their loved one was indeed dead, 2) it was beneficial for their bereavement process in that they had obtained closure in that moment, and 3) they were able to begin grieving without any unanswered questions. Post-traumatic stress symptoms are prevalent in FMs of ICU patients and may be exacerbated by their participation in end-of-life decisions without truly understanding if life has actually ended.17,18,19,20,23,31,33,36 Ongoing monitoring and research are needed on the impacts on FMs of routinely offering and witnessing of the DNC clinical assessment.

Our findings highlight the negative impacts of not making families aware of the DNC clinical assessment. Family members who were told their loved one had already been declared brain dead experienced additional confusion, stress, and grief. Nevertheless, FMs whose medical team took the time to explain the DNC clinical assessment in advance reported feeling more prepared for the determination and accepting of the result. More research is needed to explore why clinicians would not inform FMs that the clinical assessment is going to take place. While this practice may simply have been overlooked and require education on the importance to FMs, undoubtedly, there could be anxiety on the part of physicians that families may refuse the assessment or discomfort that FMs may request to be present to observe the assessment. Nevertheless, patient- and family-centred care advocates that clinicians provide family support and open lines of communication.16

Another important aspect for clinician–family communication, though not well documented in the literature, concerns the dual nature regarding time of death. Many FMs reported that the legal time of death was confusing. The time of death appears to take on a double meaning, for example, death as a moment or a state. Some FMs expressed feeling guilt in thinking their loved one died without them being present. Others noted that the confusion over the time of death was an unnecessary additional stressor during an extremely traumatic time. Some families questioned why the time of death on the death certificate was different from the time of death they had been told while in the ICU. Clinicians need to help families reconcile the legal aspect of the time of death, so families are not left with unanswered questions.

Our study has several limitations. There may be selection bias in terms of who agreed to an interview, which could be impacted by FMs who had relatively good experiences and trust in research or those who had very bad experiences and wished to express it. As such, family-generated recommendations might not apply to all and should be adapted to the individual needs of FMs. It is important to note that only a small number of families declined organ donation; hence further research is required to better understand their unique experiences. Finally, interviews were conducted with English- and French-speaking Canadian FMs only and, as a result, other ethnicity-based views have not been included.

Conclusion

In this study, we have identified important themes related to FMs’ understanding and acceptance of brain death and have identified practice-based family recommendations to address the barriers, support the facilitators, and promote more positive outcomes. These recommendations are pragmatic and can be easily implemented. Notably, we have compiled evidence on the benefits of FMs witnessing death determination, especially the apnea test. Overall, our study has provided recommendations with regard to modifiable factors such as cognitive readiness of families given their state of mind, pacing and repeating discussions according to families need to absorb, having the confidence to prepare and invite families to be present for determination to inform clinical practice, and the development of tools that can be used at the bedside. Knowledge translation tools must be developed and used selectively at the bedside depending on FMs’ needs. Ongoing qualitative research will permit better insight into minority and culturally specific experiences.