Lived Experiences of Family Members of Patients With Severe COVID-19 Who Died in Intensive Care Units in France

Key Points Question What is the experience of bereaved family members after the death of a loved one in an intensive care unit (ICU) during the first wave of the COVID-19 pandemic? Findings In this qualitative study of 19 bereaved family members, participants reported difficulties in establishing a bond with the ICU team and maintaining a relationship with their loved ones during their stay in the ICU. They also described a feeling of “stolen moments” after the death of their loved one, generating strong feelings of disbelief that could potentially lead to complicated grieving. Meaning These findings suggest that while adapting care practices and visiting policies is necessary given the public health menace, preventing families from seeing their loved ones altogether was highly detrimental: specific family-centered guidelines for crisis management are needed.


Introduction
During the initial surge of the COVID-19 pandemic, hospital visits were either banned or highly restricted, and family members were often separated from their loved ones admitted to intensive care units (ICUs). 1 Relatives were no longer allowed to be at the patient's bedside, which may have compromised their involvement in decision-making. Many clinicians felt that this situation was harmful both for patients and family members. 2,3 In this context, communication with family members was considerably modified and relied primarily on distance communication-most often via telephone, sometimes using video conferencing-potentially leading to a decrease in the quality of communication, information, and sense of support.
After a death in the ICU, bereaved family members are at high risk of presenting symptoms that can negatively impact their quality of life, such as anxiety, depression, posttraumatic stress disorder symptoms, 4,5 and complicated grief. 6 Interestingly, witnessing terminal dyspnea and not being able to say goodbye to a loved one are factors associated with increased psychological burden among relatives. 6 Thus, we speculated that the COVID-19 pandemic and the protective measures implemented in its wake may have exacerbated these negative experiences. 7 Besides these potentially complex experiences in the ICU, previous research has reported that large-scale epidemics are associated with multiple simultaneous losses, related not only to death itself but also to the disruption in social norms, end-of-life rituals, and mourning practices. 8 This may hinder the ability for individuals to connect with the deceased both before and after the death, thereby potentially increasing the risk of complicated grief. 9 Considering the limited research in this field, learning from the current COVID-19 crisis is necessary. More specifically, it is important to achieve in-depth understanding of family members' experience of the patient's stay and end of life in the ICU during the pandemic to improve practices in the future and help develop specific family-centered guidelines in times of crisis. Qualitative research is useful to shed light on the subjective experience of bereaved family members, unearth their thoughts and feelings, and improve our understanding of their needs in the context of major health crises. 10,11 Our objective in this study was to better understand the experience of family members of patients with COVID-19 who died in ICUs, from the time of admission until after the patient's death.

Methods
This qualitative study was approved by the research ethics board of Sud Méditerranée. All study participants provided oral informed consent, including permission to publish quotes. Findings are reported in accordance with Standards for Reporting Qualitative Research (SRQR) reporting guideline.

Design and Setting
This qualitative study is part of a larger quantitative multicenter study exploring the psychological burden experienced by family members of patients admitted to the ICU for COVID-19 during the initial surge of the pandemic in France (the BURDENCOV study). Briefly, participating family members were contacted 3 months after the patient's discharge or death to take part in a telephone interview to complete a questionnaire describing their experience during the patient's ICU stay, as well the Hospital Anxiety and Depression Scale and the Impact of Event Scale Revised (for symptoms of posttraumatic stress disorder). At the end of the call, family members whose relative died in the ICU were offered the opportunity to participate in the qualitative part of the study, a semistructured interview conducted a few weeks later over the telephone. Purposeful sampling was performed based on sex, age, relationship with the patient, and geographic location of the ICU so that interviewees were representative of the general population of relatives of patients in the ICU (ie, stratified sampling).

Data Collection
Interviews were conducted between June and September 2020, ie, 3 to 4 months after the patient's death. Owing to the large geographical study area and strict social distancing policies, telephone interviews were selected as the optimal method of data collection. Telephone interviews have been successfully used with bereaved relatives. 12 We used a semistructured interview guide that included the following themes: ICU admission, ICU stay, life during the patient's ICU stay, end-of-life care, funerals and rituals, and grief and mourning (eTable in the Supplement). Questions were openended, and participants were encouraged to explore issues they considered relevant. The interview guide was developed a priori by the investigators with the input of the psychologists in charge of the quantitative follow-up. Interviews were conducted in French, audio recorded, and professionally transcribed. Demographic data were self-reported and included sex, age, and relationship with the patient. Recruitment of new participants was interrupted when data saturation was reached, ie, when no new themes emerged from the interviews. 13 Although saturation was achieved at the 17th interview, we conducted 2 additional interviews beyond saturation because these family members had already agreed to participate and had their interview scheduled.

Data Analysis
Data analysis followed a 4-step process. First, 2 authors (N.K.-B. and Z.C.-S.) independently reviewed 8 randomly selected transcripts and identified key themes and concepts that occurred throughout the interviews using thematic analysis. 14 Second, a preliminary codebook was developed through an iterative process that started with the systematic comparison of the investigators' respective codes and ended when the 2 authors achieved consensus. 15 Discrepancies were resolved by discussion with a third researcher (L.M.). In the third step, the 8 initial transcripts were recoded using this codebook, and after final consolidation, a single researcher (Z.C.-S.) proceeded with the coding of the remaining interviews. The codebook contained a total of 27 codes grouped into 3 underlying themes. Finally, themes and subthemes were defined and named, and relevant quotes were selected to document and illustrate each subtheme. Data analysis was performed from August to November 2020.

Results
Among 12 ICUs located in 7 different regions of France, a total of 37 bereaved relatives were invited to participate. Among them, 9 declined, 9 could not be reached, and 19 agreed to participate in the qualitative study. The participants' characteristics are presented in Table 1

Suspended in Time and Space by New Rules
Solitude | Owing to lockdown and social distancing rules, family members were often alone while their relative was in the ICU. Loneliness was described as particularly burdensome (  Building a relationship over the telephone 1 "It was a contract that was made between the team and me: they had warned me from the start that they would call me every day at around 4 PM to check on my wife's health.… It was a landmark for me." 10 2 "They didn't call back, we had to call back every time.… You can't just leave people like that in ignorance, with their heart beating, their legs shaking, waiting for the phone call that will say that. Well, you can't do that. It's inhuman to do that." 7 3 "We were in need of explanations, I can tell you. Because my husband went to the hospital on his 2 feet, although he wasn't in good shape. Then it was just a nightmare, with no explanations.… So, then, they did take some time to help us understand, but it was too late. For me, it was too late. I didn't trust them anymore." 17 4 "The doctor called every day, but I didn't get a feeling of how my husband was really doing. It was only technical information." 14 5 "They really understood me, they showed empathy. They said, 'We know it's hard for you. This is a difficult situation. We're doing the best we can with so many patients, but we know how you've waited for this call, so we want to take the time to explain and discuss things with you.'" Solving Conflicts | Communication over the telephone was perceived as less than optimal and sometimes generated tensions or even conflicts. Participants felt that being able to meet the clinicians face to face helped to ease the situation and comfort relatives ( Table 2, quote 12).

Theme 2: the Patient in the ICU and the Risks of Separation
Among the 12 ICUs in which the participants' loved ones were hospitalized, there were 3 visiting policies: total ban on visits despite visits being exceptionally negotiated at the very end of life (3 ICUs), regular but limited visits throughout the patient's stay (5 ICUs), and end-of-life visits only (4 ICUs). These policies were felt to strongly impact family members' experiences.

Total Ban on Visits
Feeling Powerless | The total ban on visits was experienced not only as a break in the bond between the family and the patient, but also as a breaking point in the patient's perceived chances of surviving (Table 3, quote 1). In all families, the ban was associated with a very strong feeling of powerlessness (Table 3, Quote 2).
The ICU Team as an Intermediary | In a situation of total ban on visitors, the ICU team had to play the role of intermediary between the family member and the patient, which was the only way to maintain a semblance of continuity (Table 3, quote 3). When family members felt that trust in the team was broken, continuity could become problematic. Continuity | Regular visiting also was associated with continuity at the end of life and a sense of closure (Table 3, quote 6). This possibility helped family members give meaning to the patient's trajectory as well as to their own experience. Indeed, family members were able to witness and better understand the patient's deteriorating condition that led to death.

End-of-Life Visits Only
Abandonment and Unreality | For family members of patients in ICUs that only permitted visits at the end of life, the initial ban was associated with a strong feeling of abandonment (Table 3, quote   7). For some participants, reflecting on the initial ban was experienced as unreal ( Table 3, quote 8).
The Possibility of Closure | However difficult the initial restriction, the possibility of being with the patient at the time of death was paramount, since it helped both to accept the situation and to regain participants' family role (Table 3, quote 9). Participants perceived not letting the patient die alone as essential ( Table 3, quotes 10 and 13).

Frustration | When reflecting on their experience, all family members of a patient in an ICU that only
permitted end-of-life visits declared that this unique visit was insufficient (Table 3, quotes 11 and 12).
For example, one participant stated, "I asked the doctor if I could come and see him. She said, 'We "I call it the stolen moment, and by that I mean the funeral rituals. For a civilized society, such as ours, these rituals are important. In a classic death, you can accompany the deceased.… But, here, we're missing some fundamental steps in the system! My wife is alive, she goes to the hospital, she dies in the hospital, and then, on the following Friday, we're scattering her ashes." 10 14 "It's hard to grieve. Sometimes, I tell myself she will come back, it's not possible, we didn't bury her. For me, she's here, she's somewhere. I have her things at home, I didn't tidy anything up, I didn't touch anything, and everything is here." don't let families come except when we really have no hope anymore'… And what I said was, 'But this is when he needs me at his side, now more than ever, not just when there's no more hope, that's just not enough'" (Table 3, quote 11).

Theme 3: Disrupted End-of-Life Rituals and the Feeling of "Stolen Moments" With the Deceased
Before the Funeral Dehumanization | Health and safety guidelines not only kept families away from the dying person but also from the body of the deceased. Indeed, during the peak of the pandemic, relatives were forbidden access to the body: body bags were closed once and for all in the ICU. Many families described a dehumanizing experience associated with feelings of anger and injustice (Table 4, quote 1).
Not Seeing the Body: Disbelief and Ambiguity | As in disappearance cases, not seeing the body was felt to create doubt and uncertainty among bereaved family members (Table 4, quote 2). Not being able to officially identify the body was associated with profound ambiguity.

The Possibility or Impossibility of a Ceremony
For Some, No Ceremony | In some situations, ceremonies were impossible to organize (Table 4, quote 3). This absence of ceremony was associated with a feeling of guilt toward the deceased (Table 4, quote 4). All the familiar rituals, regardless of faith or religious practice, were thus missing.
New Policies and Lack of Meaning | New policies were set for ceremonies, such as an important restriction in the number of people present and the strict interdiction to touch the coffin-a rule criticized by many family members (Table 4, quote 5). These altered ceremonies lacked meaning, deprived family members of important symbolic moments, and deprived the deceased of a dignified tribute (Table 4, quotes 6 and 7).

Rituals and Grief
Classic Rituals and Adjustment to Bereavement | A very small number of families were able to organize a ceremony up to their expectations, and this was experienced as a great relief, since appropriate rituals can facilitate adjustment to bereavement. For example, one participant stated, "I fought for things to happen. And it felt good for everyone. And the battle I fought afterwards felt good for me, too. I managed to have a mass…. We scattered the ashes in the cemetery when I thought it wasn't going to be possible …. My grandchildren were able to come, although they live in different regions. That was important, very important. We were able to pay tribute to him, to talk about him" ( Table 4, quote 8).
Composing New Rituals and Moving on | In the face of numerous and drastic restrictions, some bereaved family members became proactive and found new ways of fulfilling shared rituals. Some filmed the ceremony live so that relatives could share the moment online (Table 4, quote 9). Some chose to all listen to the same music at the same time, whereas others preferred to share a moment of silence to commemorate their loved one (Table 4, quote 10). The possibility of rituals, whether classic or adapted, encouraged the bereaved to move on ( identify what was at the heart of the families' experiences during the pandemic, namely difficulties in establishing rapport and bonding with the ICU team and in understanding the information, in coping with discontinuity and interruptions in the relationship with the patient, and in dealing with the feeling of "stolen moments" after the patient's death (eFigure in the Supplement).
Over the last decades, research has shown that family members of patients receiving care in ICUs are at high risk of psychological burden. 16 Having a loved one who died or was close to death and reporting poor communication with the ICU team are 2 major risk factors. Quality of communication with the ICU team has been found to be central in shaping family members' experience, both during the patient's stay and after death. 17,18 Communication perceived as inconsistent, unsatisfactory, or uncomforting is associated with higher risk of post-ICU burden. 6,19 The risk of posttraumatic stress disorder-related symptoms increases when relatives feel that the information given is incomplete. 4 In the context of the COVID-19 pandemic, our study found that communication permits the family to understand the situation but also to feel accepted, supported, and trustful, which distant communication does not allow to the same extent. 21 Our study found that a clear information strategy was helpful but insufficient. When possible, being able to see their loved one and the care environment and interacting with the members of the ICU team helped families to better understand the patient's medical situation and feel confident that their loved one was comfortable and being well cared for.
Our study also reports that hospital visits were essential to family members in their relationship with their loved one and agrees with what family-centered research has taught us in the last 20 years: the presence of family members in ICUs should remain a priority. 22 Family members have an important role to play, 23 and their presence at the end of life is essential. Interestingly, the absence or rare presence of family members in the ICU during the pandemic has been reported as one the most difficult experiences for clinicians as well. 2 As a consequence, family-centered guidelines in times of crisis are warranted, ensuring that the place of family members in the ICU and their role at the patient's bedside are preserved.
For many family members, the notion of disappearance was felt strongly: the patient left home, was admitted to the hospital, and was never seen alive again, thereby adding even more trauma to an already traumatic experience. 24 The lack of closure for these families was notable throughout the interviews. Indeed, the ability to comfort the patient at the end of life and to say goodbye allows family members to anticipate their separation, and these are steps of crucial importance in end-oflife care rituals. 25  research is necessary to confirm the benefits of this approach. Other ways of maintaining contact could also be considered, such as writing letters or using an ICU diary, depending on cultural beliefs, practices, and values.
Lastly, our study shows that the pandemic has altered the way people grieve. Families confirmed that funerals, burials, and services were pared down, postponed, or held remotely (and with very few persons present), 29 and it was difficult to observe cultural or religious mourning practices. In fact, families were deprived of some of the most important rituals that normally occur following a death, suggesting that we are experiencing an anthropological breakdown relating to the way in which people experience dying, death, and grieving. In addition, owing to lockdown and social distancing, some family members felt isolated and alone to deal with their emotions and grief. 30,31 This context may have an impact on families' grieving, with a higher risk of developing prolonged grief. Not being able to say goodbye to their loved one, not being with the patient during dying and death, not seeing the deceased's body, and barely being able to observe common rituals may generate a sense of disbelief and doubt that may hinder the grieving process. 6

Limitations
Our study has several limitations. First, it was conducted solely in France, where care practices may not be representative of other countries, health care systems, and cultures. However, since similar measures (eg, restricted visiting policies, funeral restrictions, lockdown) were reported in most highincome countries, we believe that our results could help to understand relatives' experiences in other countries. Likewise, we used a purposive sampling strategy to maximize the diversity of family members who participated in the study. However, participation in qualitative interviews was voluntary, thus creating a possible selection bias: family members with difficulties in (or reluctance to) expressing themselves or their experiences during the pandemic may have been omitted.
Interviews were conducted early after the patient's death, making it difficult to study the bereaved families' experiences in the long term. Additionally, participants experienced losing a loved one during the first wave of the COVID-19 pandemic, at a time when hospitals were overwhelmed by the dramatic increase in cases. With time and practice, institutions have adapted to the situation, thus likely also changing bereaved family members' experiences.

Conclusions
Our qualitative study found that, in the midst of a major public health crisis, the erosion of familycentered care practices was associated with a dramatic impact on the experiences of family members of patients who died. While adapting care practices and visiting policies was undoubtedly necessary, given the nature of the threat, preventing families from seeing their loved ones altogether was also highly detrimental. To avoid traumatic experiences for patients, families, and clinicians, specific family-centered guidelines for crisis management are needed. Research in this field is required and