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Terminal Delirium: Recommendations from Bereaved Families' Experiences

Open ArchivePublished:July 28, 2007DOI:https://doi.org/10.1016/j.jpainsymman.2007.01.012

      Abstract

      Although delirium is a common complication in terminally ill cancer patients and can cause considerable distress for family members, little is known about effective care strategies for terminal delirium. The primary aims of this study were 1) to clarify the distress levels of bereaved families and their perceived necessity of care; and 2) to explore the association between these levels and family-reported professional care practice, family-reported patient behavior, and their interpretation of the causes of delirium. A multicenter questionnaire survey was conducted on 560 bereaved family members of cancer patients who developed delirium during their final two weeks in eight certified palliative care units across Japan. We obtained 402 effective responses (response rate, 72%) and, as 160 families denied delirium episodes, 242 responses were analyzed. The bereaved family members reported that they were very distressed (32%) and distressed (22%) about the experience of terminal delirium. On the other hand, 5.8% reported that considerable or much improvement was necessary, and 31% reported some improvement was necessary in the professional care they had received. More than half of the respondents had ambivalent wishes, guilt and self-blame, and worries about staying with the patient. One-fourth to one-third reported that they felt a burden concerning proxy judgments, burden to others, acceptance, and helplessness. High-level emotional distress and family-perceived necessity of improvement were associated with a younger family age; male gender; their experience of agitation and incoherent speech; their interpretation of the causes of delirium as pain/physical discomfort, medication effects, or mental weakness/death anxiety; and their perception that medical staff were not present with the family, not respecting the patient's subjective world, not explaining the expected course with daily changes, and not relieving family care burden. In terminal delirium, a considerable number of families experienced high levels of emotional distress and felt some need for improvement of the specialized palliative care service. Control of agitation symptoms with careful consideration of ambivalent family wishes, providing information about the pathology of delirium, being present with the family, respecting the patient's subjective world, explaining the expected course with daily changes, and relieving family care burden can be useful care strategies.

      Key Words

      Introduction

      Delirium or cognitive disorder occurs in 68%–90% of terminally ill cancer patients just before death.
      • Bruera E.
      • Miller J.
      • McCallion J.
      • et al.
      Cognitive failure in patients with terminal cancer. a prospective study.
      • Lawlor P.G.
      • Ganon B.
      • Mancini I.L.
      • et al.
      Occurrences, causes, and outcome of delirium in patients with advanced cancer. A prospective study.
      • Massie M.J.
      • Holland J.
      • Glass E.
      Delirium in terminally ill cancer patients.
      • Morita T.
      • Tei Y.
      • Tsunoda J.
      • et al.
      Underlying pathologies and their associations with clinical features in terminal delirium of cancer patients.
      • Pereira J.
      • Hanson J.
      • Bruera E.
      The frequency and clinical course of cognitive impairment in patients with terminal cancer.
      Although cognitive impairment can sometimes be labeled as part of the “natural” dying process, delirium-related symptoms can cause great distress to both patients and family members.
      • Breitbart W.
      • Gibson C.
      • Tremblay A.
      The delirium experience: delirium recall and delirium-related distress in hospitalized patients with cancer, their spouse/caregivers, and their nurses.
      • Morita T.
      • Hirai K.
      • Sakaguchi Y.
      • Tsuneto S.
      • Shima Y.
      Family-perceived distress from delirium-related symptoms of terminally ill cancer patients.
      According to one prospective observation study of 75 family members of delirious cancer patients, 76% of family members showed high levels of psychological distress as a result of the delirium symptoms.
      • Breitbart W.
      • Gibson C.
      • Tremblay A.
      The delirium experience: delirium recall and delirium-related distress in hospitalized patients with cancer, their spouse/caregivers, and their nurses.
      A questionnaire survey involving 300 bereaved Japanese families revealed that more than two-thirds perceived all delirium-related symptoms other than somnolence as distressing or very distressing.
      • Morita T.
      • Hirai K.
      • Sakaguchi Y.
      • Tsuneto S.
      • Shima Y.
      Family-perceived distress from delirium-related symptoms of terminally ill cancer patients.
      These results indicate that, given that one of the primary goals of integrated palliative care is to alleviate family suffering, active support for the family members of delirious terminal patients is of great importance.
      Understanding the experience of families of delirious terminally ill patients is vital to explore effective care strategies. To our knowledge, however, despite many experience-based recommendations by palliative care specialists,
      • Breitbart W.
      • Jaramillo J.R.
      • Chochinov H.M.
      Palliative and terminal care.
      • Casarett D.J.
      • Inouye S.K.
      Diagnosis and management of delirium near the end of life.
      • Kuebler K.K.
      • English N.
      • Heidrich D.E.
      Delirium, confusion, agitation, and restlessness.
      • Shuster J.
      Delirium, confusion and agitation at the end-of-life.
      only a few studies have explored the actual experiences of families in the terminal stage.
      • Susan B.
      The impact on the family of terminal restlessness and its management.
      • Pierre G.
      • Cecile C.
      • Pierre A.
      • et al.
      Delirium in advanced cancer: a psychoeducational intervention for family caregivers.

      Nanba M, Morita T, Imura C, et al. Terminal delirium: a family's live experience. Palliat Med. In press.

      Our previous qualitative study revealed that the families experienced various phenomena other than psychiatric symptoms, had a range of emotions, interpreted the delirium variously, and listed some specific useful support strategies in caring terminal delirium.

      Nanba M, Morita T, Imura C, et al. Terminal delirium: a family's live experience. Palliat Med. In press.

      Although this study provides a potentially useful insight, generalizability is limited due to a lack of quantitative data.
      The primary aim of the current study was thus to: 1) clarify the distress levels of bereaved families and their perceived necessity of care related to terminal delirium; and 2) explore the association between these levels and family-reported professional care practice, family-reported patient behavior, and their interpretation of the causes of delirium.

      Methods

      This was a cross-sectional, anonymous, multicenter survey of the bereaved families of cancer patients who had been admitted to eight palliative care units in Japan. We mailed questionnaires to bereaved families in February 2006, and again in March 2006 to nonresponding families. If the families did not want to participate in the survey, they were requested to return the questionnaire with “no participation” indicated, and the second questionnaire was not mailed. The participating institutions were conveniently selected from 150 certified palliative care units. We acknowledged the potential sampling bias, but decided to use convenient institutions due to the practical difficulties of obtaining participants from all palliative care units, and because a relatively large number of patients can minimize the risk of sampling bias.

      Subjects

      Primary palliative care responsible physicians identified potential participants following these inclusion criteria: 1) bereaved adult family members of an adult cancer patient (one family member was selected for each patient), with delirium during the final two weeks of life (based on a retrospective chart review and using Diagnostic and Statistical Manual of Mental Disorders, 4 (DSM-IV) criteria

      American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 4th ed. Washington, DC: American Psychiatric Association.

      ), 2) capable of replying to a self-reported questionnaire, 3) aware of the diagnosis of malignancy, and 4) no serious psychological distress recognized by the primary palliative care physicians. The last criterion was adopted in the same way as in our previous surveys,
      • Morita T.
      • Ikenaga M.
      • Adachi I.
      • et al.
      Family experience with palliative sedation therapy for terminally ill cancer patients.
      • Morita T.
      • Akechi T.
      • Ikenaga M.
      • et al.
      Communication about the ending of anticancer treatment and transition to palliative care.
      on the assumption that primary palliative care physicians could identify families who would suffer serious psychological distress from this survey, because they were closely involved in caring for their relative in an inpatient care setting with a mean admission period of 43 days. We excluded patients with preexisting symptomatic organic brain pathology (i.e., brain metastasis, infarction) or psychiatric disorders other than delirium (i.e., psychosis, dementia), because the psychiatric symptoms might influence the results. To minimize the possibility of sampling bias among institutions, we compared the percentages of patients diagnosed with delirium per all dead patients and the percentages of patients excluded from this study due to the last criterion among the institutions.
      Each hospital was requested to consecutively enroll the families of 90 patients who developed delirium and died in 2005 (one institution with clinical activity of less than one year enrolled all patients treated there).
      The completion and return of the questionnaire was regarded as consent to participate in this study. Ethical and scientific validity was confirmed by the institutional review board of each hospital.

      Measurement Tools

      Questionnaire

      A questionnaire (available from the authors upon request) was developed for this study based on a systematic literature review,
      • Breitbart W.
      • Gibson C.
      • Tremblay A.
      The delirium experience: delirium recall and delirium-related distress in hospitalized patients with cancer, their spouse/caregivers, and their nurses.
      • Morita T.
      • Hirai K.
      • Sakaguchi Y.
      • Tsuneto S.
      • Shima Y.
      Family-perceived distress from delirium-related symptoms of terminally ill cancer patients.
      • Breitbart W.
      • Jaramillo J.R.
      • Chochinov H.M.
      Palliative and terminal care.
      • Casarett D.J.
      • Inouye S.K.
      Diagnosis and management of delirium near the end of life.
      • Kuebler K.K.
      • English N.
      • Heidrich D.E.
      Delirium, confusion, agitation, and restlessness.
      • Shuster J.
      Delirium, confusion and agitation at the end-of-life.
      • Susan B.
      The impact on the family of terminal restlessness and its management.
      • Pierre G.
      • Cecile C.
      • Pierre A.
      • et al.
      Delirium in advanced cancer: a psychoeducational intervention for family caregivers.

      Nanba M, Morita T, Imura C, et al. Terminal delirium: a family's live experience. Palliat Med. In press.

      • Anetth G.
      • Ingegerd B.E.
      • Dag L.
      Patients' experience of being critically ill or severely injured and cared for in an intensive care unit in relation to the ICU syndrome.
      • Brigit R.
      • Wendy C.
      Patients' dreams and unreal experiences following intensive care unit admission.
      • Cynthia M.
      • Sherill N.C.
      Delirium: elders tell their stories and guide nursing practice.
      • Edith M.A.
      • Ingalill R.H.
      • Astrid N.
      • et al.
      The meaning of acute confusional state from the perspective of elderly patients.
      • Fagerberg I.
      • Jonhagen M.E.
      Temporary confusion: a fearful experience.
      • Irene S.
      A small exploratory study of the reaction of older people to an episode of delirium.
      our previous qualitative study based on in-depth interviews with 20 bereaved family members,

      Nanba M, Morita T, Imura C, et al. Terminal delirium: a family's live experience. Palliat Med. In press.

      and discussions among the authors. Content validity was assessed by full agreement of the authors, and the face validity of the questionnaire was confirmed by a pilot test.
      As background data, the families reported their ages, genders, relationships to the patient, and intervals from patient death to the study. In the first part of the questionnaire, we asked the respondents whether they thought the patient was delirious or not, because in our previous interview study, 17 of 37 families denied delirium despite diagnostic confirmation based on chart review.

      Nanba M, Morita T, Imura C, et al. Terminal delirium: a family's live experience. Palliat Med. In press.

      Delirium was paraphrased in the questionnaire as “the rapid development of difficulty in concentration, forgetfulness, disorientation about time and place, hallucinations and delusions, incoherent speech, clouding of consciousness and difficulty in communicating, emotional instability, reversal of daytime and nighttime activities (drowsiness during the day and wakefulness during the night), and inconsistent behavior, with these conditions changing even within a day.” We carefully developed this introduction section on the basis of the DSM-IV criteria through full agreement among the author liaison psychiatrists and palliative care specialists.
      The primary endpoints of this study were family-perceived emotional distress related to terminal delirium and the necessity for improvement in professional care at that time. Due to the lack of validated instruments, these outcome parameters were developed for this study following previous surveys.
      • Morita T.
      • Ikenaga M.
      • Adachi I.
      • et al.
      Family experience with palliative sedation therapy for terminally ill cancer patients.
      • Morita T.
      • Akechi T.
      • Ikenaga M.
      • et al.
      Communication about the ending of anticancer treatment and transition to palliative care.
      The level of family-perceived distress was evaluated by the response to “How distressing was the patient's delirium for you?,” rated on a 5-point scale from 1, “no distress at all” to 5, “very distressing.” The necessity for improvement was evaluated by the answer to “How much improvement do you think is necessary in the care for delirium?,” rated on a 4-point scale as 1, “no need for improvement,” 2, “need for some improvement,” 3, “need for considerable improvement,” and 4, “need for much improvement.” To explore the families' emotions, we asked the respondents to rate their degree of agreement with 16 statements to describe their feelings on a 5-point Likert-type scale of 1, “disagree,” to 5, “strongly agree” (Table 2). In addition, we asked the respondents to rate their degree of agreement with eight potential meanings of delirium for the family member on a 5-point Likert-type scale of 1, “disagree,” to 5, “strongly agree” (Table 4).
      The families were further requested to report factors potentially contributing to these primary endpoints. They were conceptualized prior to the survey and classified into the following categories: 1) family-reported patient behavior (rated on a 5-point Likert-type scale of 1: none, 2: occasionally, and 3: often) (Table 3); 2) families' interpretation of the causes of delirium (examined by the degree of agreement on a 5-point Likert-type scale of 1: disagree to 5: strongly agree) (Table 4); 3) family-reported professional care practice (examined using the yes-no format) (Table 5); and 4) the family care subscale of the Care Evaluation Scale.
      • Morita T.
      • Hirai K.
      • Sakaguchi Y.
      • et al.
      Measuring the quality of structure and process in end-of-life care from the bereaved family perspectives.
      The Care Evaluation Scale is an originally validated 28-item questionnaire to measure bereaved family-perceived necessity of improvement in end-of-life care;
      • Morita T.
      • Hirai K.
      • Sakaguchi Y.
      • et al.
      Measuring the quality of structure and process in end-of-life care from the bereaved family perspectives.
      its reliability and validity have been well established. The family care subscale was designed to quantify the family-perceived necessity of improvement in care to relieve the family care burden. A lower score indicated a greater need for improvement (possible range, 0–10).

      Chart Review Data

      Primary palliative care physicians recorded the patient backgrounds (age, gender, primary tumor site, admission periods, and the type and severity of delirium on item 9 of the Memorial Delirium Assessment Scale—Japanese version
      • Matsuoka Y.
      • Miyake Y.
      • Arakaki H.
      • et al.
      Clinical utility and validation of the Japanese version of Memorial Delirium Assessment Scale in a psychogeriatric inpatient setting.
      ).

      Analyses

      To describe the estimated frequency of the phenomenon observed, we calculated the 95% confidence intervals (CI) for each figure.
      For comparisons, the respondents were classified into two groups: family members who rated their distress level as “very distressed” (high-level distress) and others (low-level distress); and family members who rated the necessity for improvement as “much,” “considerable,” or “some” (defined as a high level of perceived necessity for improvement) and others (low level). These cutoff points were determined on the basis of the actual data distribution to divide the whole sample into appropriate sizes of comparison groups.
      To explore the underlying structure of the families' emotions (Table 2), we reported factor-loading values by exploratory factor analysis with promax rotation on emotion-related items, and calculated Cronbach's alpha. Two ambivalent items with different meanings within one sentence were excluded from this analysis.
      To explore the determinants of the levels of family-perceived distress and necessity for improvement, we initially screened: 1) demographic variables (patient age, gender, admission periods, responding family member age, gender, relationship to the patient, interval from patient death to study, health status in the last week, availability of someone with whom they could consult about the patient, and someone who could care for the patient instead of them); 2) type and severity of delirium (measured using item 9 of the Memorial Delirium Assessment Scale by the primary physicians); 3) family-reported patient behavior (Table 3); 4) families' interpretation of the causes of delirium (Table 4); 5) family-reported professional care practice (Table 5); and 6) the family care subscale of the Care Evaluation Scale. Univariate analyses were performed using Student's t-test or the Chi-square test, where appropriate. Multiple logistic regression analyses were then performed in a forward-elimination fashion. All potential predictors with statistical significance by univariate analyses were entered in the equation as independent variables, and we reported the factors that achieved P<0.1 because they had a clinically meaningful interpretation despite marginal statistical significance.
      All analyses were performed using the Statistical Package for the Social Sciences (version 11.0).

      Results

      Of 984 patients who died during this study period, 672 patients (68%) were diagnosed with delirium during the final two weeks of life. Of them, 53 patients had preexisting symptomatic organic brain or psychiatric disorders, and 19 patients had no competent adult family members available. Of the remaining 600 patients, we excluded 40 bereaved family members (6.7%) due to serious psychological distress recognized by primary physicians. Among the institutions, the percentages of patients diagnosed with delirium per all deceased patients ranged from 47% to 87% (three institutions below 70%), and the percentages of patients excluded from this study due to psychological reasons ranged from 0% to 12% (all but one institution below 7.0%).
      We thus sent questionnaires to 560 families, 10 of which were returned as undeliverable. Four hundred twenty-seven families returned questionnaires (response rate, 78%, 427/550). Of them, nine families refused to participate, and 16 responses were excluded due to missing data in primary endpoints. Thus, we obtained 402 effective responses (effective response rate, 73%, 402/550). As 160 families denied delirium episodes, further analyses were performed on 242 responses. Table 1 summarizes the backgrounds of patients and bereaved family members. The subtypes of delirium were hypoactive, 29% (n=70); hyperactive, 48% (n=117); and mixed, 20% (n=48). Symptom severity was mild, 39% (n=95); moderate, 47% (n=114); and severe, 11% (n=26) on item 9 of the Memorial Delirium Assessment Scale.
      Table 1Backgrounds
      % (n)
      Patients
      Age (mean±SD)69±12
      Sex
       Male64 (155)
       Female36 (87)
      Primary sites
       Lung26 (62)
       Stomach13 (31)
       Colon, rectum11 (27)
       Pancreas, bile duct12 (29)
       Liver5.3 (13)
       Neck6.2 (15)
       Uterus, ovary4.1 (10)
       Bladder, kidney, prostate7.9 (19)
       Breast3.3 (8)
       Esophagus2.5 (6)
       Unknown2.1 (5)
       Others7.0 (17)
      Admission periods (d) (mean±SD)43±48 (median, 28)
      Bereaved families
      Age (mean±SD)58±13
      Sex
       Male25 (60)
       Female74 (178)
      Relationship
       Spouse55 (132)
       Child30 (72)
       Parents1.7 (4)
       Siblings4.1 (10)
       Others9.1 (22)
      Interval from patient death (mo) (mean±SD)12±13 (median, 11)
      In the last week
      Health status
       Good74 (180)
       Poor24 (58)
      Availability of person with whom the respondent consulted about the patient91 (221)
      Availability of person who cared for the patient instead of the respondent71 (171)
      Frequency of staying with the patient
       Every day77 (186)
       4–6 days/wk12 (29)
       1–3 days/wk8.7 (21)
      Some data do not add up to 100% due to missing values.

      Overall Levels of Family-Reported Distress and Necessity for Improvement

      The degree of family-reported distress was very distressing (32% [95% CI: 26,38], n=77), distressing (22% [95% CI: 17,28], n=53), slightly distressing (31% [95% CI: 25,37], n=74), not so distressing (10% [95% CI: 7.0,15], n=25), and not distressing at all (5.4% [95% CI: 3.0-9.0], n=13). The necessity of improvement in delirium care as rated by the family members was much improvement needed (0.8% [95% CI: 0,3.0], n=2), considerable improvement needed (5.0% [95% CI: 3.0,9.0], n=12), some improvement needed (31% [95% CI: 25,37], n=75), and no improvement needed (59% [95% CI: 53,65], n=143).

      Family-Reported Emotions

      Exploratory factor analysis categorized family-reported emotions into seven categories: ambivalent, guilt and self-blame, worry about staying with the patient, burden about proxy judgment, burden to others, acceptance, helplessness, and relief. More than half of the respondents had ambivalent wishes, guilt and self-blame, and worries about staying with the patient. One-fourth to one-third reported that they felt a burden over proxy judgments, burden to others, acceptance, and helplessness. Less than 5% reported positive feelings such as relief (Table 2).
      Table 2Family-Reported Emotions
      Agree or Strongly Agree95% CIFactor LoadingsAlpha
      % (n)
      AmbivalentN.C.
       Simultaneously wanted the patient both to stay awake and to relieve the patient from suffering.64 (155)58,70N.C.
       Simultaneously wanted the patient both to live longer and to die without suffering.40 (97)34,46N.C.
      Guilt and self-blame0.87
       Could not understand what the patient wished for.62 (149)55,680.89
       Might not be able to realize the patient's unfulfilled wishes.56 (135)49,620.89
       Guilty, could not do enough for the patient.52 (126)46,580.88
      Worry about staying with the patient0.77
       Worried about caring the patient alone.58 (140)51,640.89
       Anxious about taking their eyes off the patient.57 (139)51,640.88
      Burden about proxy judgmentN.C.
       Burden about having to make a decision on behalf of the patient.39 (94)33,450.86
      Burden to others0.60
       Distressed as the patient troubled others.38 (91)32,440.68
       Not wanting other members of the family to see the patient.35 (84)29,410.69
       Sad to see the patient having completely changed.29 (71)24,350.85
      AcceptanceN.C.
       Just accepting the fact.35 (84)29,410.96
      Helplessness0.78
       Helplessness about what to do.32 (78)27,380.87
       Not sure about what was happening.28 (68)23,340.91
      Relief0.81
       Felt relieved.3.3 (8)2.0,6.00.89
       Felt happy.2.5 (6)1.0,5.00.91
      N.C. = not calculated.

      Family-Reported Patient Behavior

      The bereaved family members reported various patient behaviors other than “psychiatric symptoms.” More than half of the respondents reported that, during the delirium episodes, the patient expressed physiologic desires, seemed incoherent but talked about actual past events, and talked about uncompleted life tasks. In addition, about 30% said that the patient apologized for past events and was distressed as they noticed that they were talking strangely. About 20% of the family members reported a transcendent experience, that is, that the patient talked to or met people who had died (Table 3).
      Table 3Family-Reported Patient Behavior in the Delirium Episodes
      Occasionally95% CIOften95% CI
      % (n)% (n)
      “Psychiatric symptoms”
       Incoherent speech53 (128)47, 5925 (60)20, 31
       Mentally clear in some situations within the day36 (88)31, 4337 (89)31, 43
       Hallucinations34 (83)29, 4117 (40)12, 22
       Agitated behavior31 (75)25, 3715 (36)11, 20
      Other than “psychiatric symptoms”
       Expressed physiologic desires (excretion, thirst)31 (76)26, 3840 (96)34, 46
       Seemed incoherent but talked about actual past events41 (100)35, 4826 (62)20, 32
       Talked about uncompleted life tasks32 (78)27, 3824 (57)19, 29
       Good mood33 (80)27, 397.4 (18)5.0, 11
       Apologized for past events22 (53)17, 286.6 (16)4.0, 11
       Distressed as the patient noticed him/herself talking strangely21 (51)16, 276.6 (16)4.0, 11
       Said that the patient talked to or met people who had died18 (44)14, 244.1 (10)2.0, 7.0

      Family-Perceived Meaning of Delirium and Interpretation of the Causes of Delirium

      About half of the respondents perceived delirium as a sign of approaching death, the patient trying to express what to say, or patient suffering. About one-fourth to one-third perceived delirium as a natural part of the dying process, dreaming, a transcendent phenomenon (entering the after-death world), or relief from actual suffering. Forty to 60% of the families interpreted the causes of delirium as pain/physical discomfort or medication effects (Table 4).
      Table 4Family-Perceived Meaning of Delirium and Interpretations About the Causes of Delirium
      Agree, or Strongly Agree95% CI
      % (n)
      Meaning of delirium
       Sign of approaching death59 (143)53, 65
       Trying to express what the patient wanted to do or say52 (125)45, 58
       Suffering45 (108)38, 51
       A natural part of the dying process31 (74)25, 37
       Dream25 (61)20, 31
       Entering after-death world22 (54)17, 28
       Relief from actual suffering22 (53)17, 28
       Happy and welcome experience7.0 (17)4.0, 11
      Interpretation about the causes of delirium
       Pain or physical discomfort60 (144)53, 66
       Medication effects41 (99)35, 47
       Psychosis or “becoming crazy”19 (46)15, 24
       Mental weakness or death anxiety15 (37)11, 20

      Family-Reported Professional Care Practice for Delirium

      The families generally reported high adherence to the recommended care practice for terminal delirium. Eighty percent or more families agreed that professionals treated patients the same as before, tried to understand what the patient wanted to say, were sufficiently compassionate to the family, explained the expected course along with daily changes, and respected the patient's subjective world (Table 5).
      Table 5Family-Reported Professional Care Practice for Delirium
      Practiced95% CI
      % (n)
      Treated patients the same as before94 (227)90, 96
      Tried to understand what the patient wanted to say88 (214)84, 92
      Was sufficiently compassionate to the family86 (208)81, 90
      Explained the expected course along with daily changes86 (207)80, 89
      Respected the patient's subjective world without denying “incoherent things”83 (202)78, 88
      Discussed with the family about how to deal with the issue75 (181)69, 80
      Explained the pathology of delirium (not dementia or psychosis)72 (175)66, 78
      Was present with the family71 (173)65, 77
      Facilitated with family members in communicating and being with the patient before it became difficult68 (164)62, 73
      Explained the universality of delirium66 (159)59, 71
      Confirmed the patient's wishes before communication became difficult54 (131)48, 60
      Physical restraint
       Before admission to palliative care units3.3 (8)2.0, 6.0
       In palliative care units2.5 (6)1.0, 5.0

      Determinants of Family-Perceived Emotional Distress and Necessity of Improvement

      Compared with the family members with low-level distress, family members with high-level distress were more likely to experience agitated behavior, incoherent speech, the patient talking about uncompleted life tasks, the patient appearing incoherent but talking about actual past events, and being distressed by noticing that they were talking strangely; more likely to interpret the causes of delirium as pain/physical discomfort, medication effects, psychosis/“getting crazy,” and mental weakness/death anxiety; less likely to report the medical professionals as present with the family; and more likely to report the patient being physically restrained (Table 6).
      Table 6Determinants of Family-Reported Emotional Distress and Necessity of Improvement
      Emotional Distress LevelNecessity of Improvement
      Univariate AnalysesMultivariate Analysis
      R2=0.15.
      Univariate AnalysesMultivariate Analysis
      R2=0.37.
      High-Distress (n=77)Low-Distress (n=165)Odds Ratio [95% CI]PHigh Necessity (n=89)Low Necessity (n=143)Odds Ratio [95% CI]P
      Background
       Age (family)55±1160±14
      P<0.05.
      0.96 [0.93–0.99]0.016
       Sex (family, female)64% (n=57)79% (n=113)
      P<0.05.
      0.22 [0.096–0.50]0.001
       Sex (patient, female)45% (n=40)31% (n=44)
      P<0.05.
      Family-reported patient behavior
      Rated as 0 (none), 1 (occasionally), and 2 (often).
       Agitated behavior0.85±0.780.51±0.69
      P<0.001.
      1.5 [0.98–2.4]0.063
       Incoherent speech1.2±0.720.97±0.64
      P<0.01.
      1.7 [1.0–2.9]0.042
       Talked about uncompleted life tasks1.0±0.830.73±0.77
      P<0.01.
       Seemed incoherent but talked about actual past events1.2±0.720.90±0.76
      P<0.05.
       Distressed as the patient noticed0.49±0.730.30±0.53
      P<0.05.
      Interpretations of the causes
      Rated as 0 (strongly disagree) to 4 (strongly agree).
       Pain or physical discomfort3.0±1.32.5±1.2
      P<0.01.
      1.3 [0.95–1.7]0.0992.9±1.22.5±1.2
      P<0.05.
       Medication effects2.3±1.22.0±1.2
      P<0.05.
      2.4±1.11.9±1.200
      P<0.01.
      1.5 [1.1–2.1]0.014
       Mental weakness or death anxiety1.6±1.31.3±0.94
      P<0.05.
      1.3 [0.97–1.8]0.078
       Psychosis or “getting crazy”1.6±1.31.3±1.1
      P<0.05.
      Family-reported professional care
      Rated as practiced or not.
       Was present with the family62% (n=48)76% (n=125)
      P<0.05.
      0.49 [0.23–1.0]0.06858% (n=52)83% (n=119)
      P<0.001.
      0.35 [0.12–1.0]0.053
       Respected the patient's subjective world81% (n=72)88% (n=126)
      P<0.05.
      0.16 [0.019–1.3]0.088
       Explained the expected course79% (n=70)92% (n=132)
      P<0.01.
      0.13 [0.028–0.64]0.011
       Tried to understand what the patient said87% (n=77)93% (n=133)
      P<0.001.
       Was sufficiently compassionate to the family76% (n=68)93% (n=133)
      P<0.001.
       Had confirmed the patient's wishes before communication became difficult44% (n=39)64% (n=91)
      P<0.001.
       Had facilitated communication before it became difficult62% (n=55)73% (n=105)
      P<0.01.
       Relieved the family care burden
      Rated on the family care subscale of the Care Evaluation Questionnaire. Lower score indicates a family-perceived higher necessity of care to relieve the family care burden.
      6.4±2.57.9±2.5
      P<0.001.
      0.84 [0.73–0.98]0.025
       Physical restraint10% (n=8)3.6% (n=6)
      P<0.05.
      a R2=0.15.
      b R2=0.37.
      c P<0.05.
      d Rated as 0 (none), 1 (occasionally), and 2 (often).
      e P<0.001.
      f P<0.01.
      g Rated as 0 (strongly disagree) to 4 (strongly agree).
      h Rated as practiced or not.
      i Rated on the family care subscale of the Care Evaluation Questionnaire. Lower score indicates a family-perceived higher necessity of care to relieve the family care burden.
      Compared with the family members who perceived a low-level necessity of improvement, family members who perceived a high-level necessity of improvement were more likely to be young and male; more likely to interpret the causes of delirium as pain/physical discomfort and medication effects; less likely to report that the medical professionals were present with the family, respected the patient's subjective world, explained the expected course along with daily changes, tried to understand what the patient wanted to say, were sufficiently compassionate to the family, had facilitated communication before it became difficult, and had confirmed the patient's wishes before communication become difficult; and reported a lower score of the family care subscale of the Care Evaluation Scale.
      Multiple logistic regression analyses revealed that the independent determinants of high-level distress or high-level necessity of improvement were younger age; male gender; experience of agitation and incoherent speech; interpretation of the causes of delirium as pain/physical discomfort, medication effects, or mental weakness/death anxiety; and medical staff being present with the family, respecting the patient's subjective world, explaining the expected course along with daily changes, and relieving the family care burden.

      Discussion

      This is, to our knowledge, the first systemic survey to investigate the potential correlations of the distress levels of families and the perceived necessity of improvement in care related to terminal delirium with family-reported professional care practice, family-reported patient behavior, and perception of the causes of delirium.
      This survey revealed that, although a relatively small number of families (5.8%) reported that considerable or much improvement was necessary in the professional care they had received in certified palliative care units, about half of the families reported being very distressed or distressed about the experience of terminal delirium. This figure is relatively low compared with the previous two surveys,
      • Breitbart W.
      • Gibson C.
      • Tremblay A.
      The delirium experience: delirium recall and delirium-related distress in hospitalized patients with cancer, their spouse/caregivers, and their nurses.
      • Morita T.
      • Hirai K.
      • Sakaguchi Y.
      • Tsuneto S.
      • Shima Y.
      Family-perceived distress from delirium-related symptoms of terminally ill cancer patients.
      but confirms that at least 50% of the families of patients with delirium experienced considerable emotional distress.
      The most important finding of this study was the identification of factors associated with the distress levels of families and their perceived necessity of improvement. The chief factors included family experience of agitation, their interpretation of the causes of delirium, and their perception about the care they had received.
      Consistent with previous surveys that identified agitation as a significant determinant of family distress,
      • Breitbart W.
      • Gibson C.
      • Tremblay A.
      The delirium experience: delirium recall and delirium-related distress in hospitalized patients with cancer, their spouse/caregivers, and their nurses.
      • Morita T.
      • Hirai K.
      • Sakaguchi Y.
      • Tsuneto S.
      • Shima Y.
      Family-perceived distress from delirium-related symptoms of terminally ill cancer patients.
      family-reported agitation was an important determinant of family distress in this study. The control of agitation symptoms, therefore, is an important task for palliative care clinicians. This study revealed, however, that ambivalent wishes between symptom control and maintaining communication were the most common emotions of the families. Together with qualitative studies stressing the importance of ambivalent wishes in this situation,
      • Susan B.
      The impact on the family of terminal restlessness and its management.

      Nanba M, Morita T, Imura C, et al. Terminal delirium: a family's live experience. Palliat Med. In press.

      clinicians should note that families want not only symptom palliation but also much broader elements of quality of life, such as maintaining cognitive control, communicating with others, and living as long as possible.
      • Steinhauser K.E.
      • Christakis N.A.
      • Clipp E.C.
      • et al.
      Factors considered important at the end of life by patients, family, physicians, and other care providers.
      • Hirai K.
      • Miyashita M.
      • Morita T.
      • et al.
      Good death in Japanese cancer care: a qualitative study.
      That is, clinically, pharmacologically sedative therapy should not be routinely applied to control agitation symptoms without careful individualized considerations, and the depth or duration of sedation should be closely adjusted for each situation.
      • Morita T.
      • Bito S.
      • Kurihara Y.
      • Uchitomi Y.
      Development of a clinical guideline for palliative sedation therapy using the Delphi method.
      Families often interpreted delirium as the consequences of pain/physical discomfort, medication effects, psychosis/“becoming crazy,” or mental weakness/death anxiety, and these interpretations were significantly associated with both family distress and necessity of improvement. These findings confirm the great importance of information focusing on the cause and pathologies of delirium (i.e., terminal delirium is usually not an expression of pain, medication effects, “becoming crazy,” or mental weakness), as stated in expert literature.
      • Kuebler K.K.
      • English N.
      • Heidrich D.E.
      Delirium, confusion, agitation, and restlessness.

      Nanba M, Morita T, Imura C, et al. Terminal delirium: a family's live experience. Palliat Med. In press.

      The major care practices related to a family's emotional distress and necessity of improvement included being present with the family, respecting the patient's subjective world, explaining the expected course with daily changes, and relieving the family care burden.
      Of special note, as this study suggests, respecting the patient's subjective world can be an important care strategy in terminal delirium. This care strategy was associated with the overall necessity of improvement, and the family members experienced various patient behaviors other than “psychiatric symptoms”: the patient expressed physiologic desires, seemed incoherent but talked about actual past events, talked about uncompleted life tasks, and apologized for past events. Consistent with the recommendations of palliative care textbooks,
      • Breitbart W.
      • Jaramillo J.R.
      • Chochinov H.M.
      Palliative and terminal care.
      • Casarett D.J.
      • Inouye S.K.
      Diagnosis and management of delirium near the end of life.
      • Kuebler K.K.
      • English N.
      • Heidrich D.E.
      Delirium, confusion, agitation, and restlessness.
      • Shuster J.
      Delirium, confusion and agitation at the end-of-life.
      these findings suggest that the care strategy for terminal delirium may include exploring and fulfilling unmet physiological needs behind delirium symptoms, and trying to understand the “strange” behavior of delirious patients as a potentially meaningful experience to find a clue for important landmark events and achieve uncompleted life tasks for patients and families.
      Among care strategies investigated in this study, only being with the patient was associated with families' emotional distress. This result indicates, as nonempirical literature stresses the importance of “being” for palliative care clinicians,
      • Breitbart W.
      • Jaramillo J.R.
      • Chochinov H.M.
      Palliative and terminal care.
      • Casarett D.J.
      • Inouye S.K.
      Diagnosis and management of delirium near the end of life.
      • Kuebler K.K.
      • English N.
      • Heidrich D.E.
      Delirium, confusion, agitation, and restlessness.
      • Shuster J.
      Delirium, confusion and agitation at the end-of-life.
      being with the families of delirious patients is an essential element of care.
      The family-perceived necessity of improvement in care to relieve the family care burden was a significant determinant in the overall family-perceived necessity of improvement. As the family is an important target in palliative care, clinicians should make maximum efforts to relieve the family care burden, through reassuring the families that they can leave the patients' care to the staff, making the hospital environment comfortable for the families, and coordinating support from other members of the family.
      Of interest was that this study highlighted some specific emotions evoked by the experience of terminal delirium. In this study sample, the three major emotions were ambivalent wishes, guilt and self-blame, and worry about staying with the patient. As only a few qualitative studies proposed a care strategy to relieve such specific distress,

      Nanba M, Morita T, Imura C, et al. Terminal delirium: a family's live experience. Palliat Med. In press.

      more empirical studies are needed to understand in-depth family emotions related to terminal delirium and explore a specific care strategy.
      Despite several strengths, including the success in obtaining a large sample with more than a 70% response rate, this study has some limitations. First, due to its retrospective nature, there might be a recall bias. Second, some families denied the episode of delirium despite a psychiatrically confirmed diagnosis, and might recall episodes other than delirium. Third, as all patients received specialized palliative care, adherence levels to recommended care practice were generally high and might result in low-sensitivity statistical analyses, and the findings could not be automatically generalized to other situations. Fourth, the cross-sectional design of this study cannot allow the causality of the associations identified. Fifth, we excluded 6.7% of the potential respondents with profound emotional distress due to ethical reasons. Finally, what is important for a good death, such as maintaining consciousness and dying during sleep, is different among cultural backgrounds,
      • Hirai K.
      • Miyashita M.
      • Morita T.
      • et al.
      Good death in Japanese cancer care: a qualitative study.
      • Fainsinger R.L.
      • Nunez-Olarte J.M.
      • Demoissac D.M.
      The cultural differences in perceived value of disclosure and cognition: Spain and Canada.
      and the results might not be automatically applied to different cultural settings.
      In conclusion, a considerable number of family members experienced high levels of emotional distress and felt some need for improvement of the care for terminal delirium. Control of agitation symptoms with careful consideration of ambivalent family wishes, information about the pathophysiology of delirium, being present with the family, respecting the patient's subjective world, explaining the expected course with daily changes, and relieving the family care burden can be useful care strategies. Intervention trials to determine the efficacy of these care strategies are needed.

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