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Abstract
Objective Caregivers to patients with primary malignant brain tumours neglect their own physical and emotional needs during the disease trajectory. The aim of the systematic review was to explore how informal caregivers of patients with primary malignant brain tumour (high-grade glioma (HGG)) experience and manage their life situation after the death of the patient.
Methods A systematic literature search was carried out in December 2016 and revised in September 2017. The following six databases were searched: PubMed, Cumulative Index of Nursing and Allied Health Literature, Excerpta Medica database, Scopus, PsycINFO and The Social Sciences Citation Index. Studies eligible for inclusion met the following criteria: (1) included bereaved caregivers to patients diagnosed with HGG ≥18 years, (2) described the caregiver’s perspective at post bereavement (3) had been peer-reviewed. The papers included were assessed for methodological quality using the Critical Appraisal Skills Programme.
Results Four qualitative articles, published from 2004 to 2015, met the eligibility criteria. Bereaved informal caregivers expressed profound grief and had unmet needs and questions related to the disease and their role as caregiver. Moreover, they experienced depressive symptoms and fatigue, resulting in a reduced work capability and social network.
Conclusions We conclude that bereaved informal caregivers experience psychosocial consequences and emotional reactions after bereavement, resulting in feelings of isolation and loneliness. This review identified limited evidence on how the bereaved caregivers prefer to be supported, and further study is warranted. We suggest incorporating systematic information on bereavement in clinical practice and a cooperation across sectors.
- brain
- bereavement
- caregiver
- bereaved
- end of life care
- primary malignant brain tumour
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Background
Primary malignant brain tumour (PMBT) is a life-threatening diagnosis with a 5-year survival rate of 10%.1 In 2013, the incidence of PMBT was 5.1% in developed countries.2 PMBT diagnoses differ from other types of cancer due to the severe symptom burden caused by the tumours’ invasive growth into the surrounding brain tissue. Symptoms, which vary depending on the tumour’s size and location,3 can be physical (hemiparesis, aphasia and seizures), psychosocial (stress, anxiety and depression) and cognitive (personality changes, concentration problems and reduced attention span and short-term memory).4 5 PMBT covers different subtypes of malignant brain tumours. According to WHO, grade III and IV tumours are pathologically classified as high-grade glioma (HGG), including glioblastomas (GBM), anaplastic astrocytoma (AA) and anaplastic oligodendroglioma (AO).6 In general, patients with WHO grade III tumours (AA and AO) have a more optimal prognosis than patients diagnosed with GBM (WHO grade IV), but still progress with a similar course.
During the HGG disease and treatment trajectory, the patient is highly influenced by various and increasing symptoms, with fatigue, aphasia and reduced consciousness reported as the three most common symptoms.7 Current standard treatment consists of surgery followed by radiotherapy with concomitant and adjuvant chemotherapy over the course of a year.1 This life-prolonging treatment has increased survival from 12.1 to 14.6 months.1
An HGG diagnosis and subsequent treatments result in profound changes, not only for the patient, but also within the affected families.8 9 It is well known that the closest relatives often become the primary caregivers.10 For some relatives, the role from family member to caregiver occurs at the time of diagnosis, while for others these changes occur later. The patient’s complex symptoms and need for support and assistance often lead to a change in family roles.3 Caregivers often describe cognitive changes as the greatest challenge, and they feel inadequately prepared to handle these changes adequately.3 10 11 Taking on the caregiver role leads to a loss of equality in the relationship, and caregivers therefore express the feeling that they have lost their partner.8
Caregivers often experience a process of crisis and grief3 because they live in a constant state of anxiety and fear of losing the patient.12 While the patient’s symptoms gradually become more severe, the caregiver burden increases. Meanwhile, patients and the caregivers have to cope with the difficult issue of death approaching.3 10 12 Moreover, caregivers suffer from lack of sleep12 and often feel isolated.10 Both patients and caregivers are at risk of developing depression.5 13 14 In particular, caregivers are at increased risk of developing depression due to a reduction in resources due to lack of energy and grief.15 Additionally, caregivers often have to handle the patient’s depressive thoughts and negative emotions, a task reported as being more taxing than providing physical care.10 In general, caregivers tend to neglect their own physical and emotional needs as they prioritise other tasks, including economy, household chores, work, role changes and adjustment within the family.10
HGG is often characterised by rapid disease progression, with the patient moving through the phases very quickly, in some cases skipping the stable or chronic phase and going directly from diagnosis to the end of life (EOL).10 The supportive care needs of caregivers vary across time and are affected by the amount of time they have to adjust or adapt to the patient’s changed situation.10 Caregivers might suffer from a sense of powerlessness derived from being unable to influence the patient’s situation.12 In some cases, the patient and the caregiver had already taken action and planned for an EOL period which was different to what actually happened. An Australian report shows that 26% of patients with PMBT die outside of hospital, 49% in a palliative or hospice setting and 25% in an acute hospital bed.16 In the event that EOL has not been discussed and/or wishes surrounding death were not met, bereaved caregivers may be negatively impacted. The National Comprehensive Cancer Network (NCCN) from the USA provides interdisciplinary recommendations on palliative care for patients with cancer.17 It is recommended to carry out a postbereavement intervention for bereaved family and caregivers.17 The development of guidelines is facilitated by leading American cancer centres and requested internationally. However, the present NCCN guidelines on central nervous system cancers focus primarily on treatment and control related to disease progression and side effects.18 Presently, there is a lack of evidence to suggest which type of support the bereaved caregivers may benefit from. Hence, the main implication of the current review includes an increased knowledge on the life situation of bereaved caregivers to establish future interventions that aim to address their needs and key concerns. The aim of this systematic review is to provide an overview of the literature that explores how caregivers of patients with HGG experience and manage their life situation following the death of the patient.
Methods
Literature search
A literature search was conducted by a research information specialist on 15 December 2016 in PubMed and 16 December 2016 and then revised on 29 September 2017 in six databases: PubMed, Cumulative Index of Nursing and Allied Health Literature (CINAHL), Excerpta Medica database, The Social Sciences Citation Index (SSCI), Scopus and PsycINFO. A combination of controlled vocabulary and free-text terms was used. Figure 1 illustrates the search strategy from September 2017. Covidence software was applied to identify duplicates, screen-imported studies and maintain the structure of the process. Two investigators (KP, SN) separately conducted the evaluation of the imported literature based on the title and abstract, and undertook the full-text review. In case of doubt, the paper was re-read and discussed between the reviewers with the opportunity to invite a third researcher (MJ) to join the discussion. Further, authors of relevant conference abstracts were contacted by email to clarify whether they had published peer-reviewed papers that might be eligible for inclusion. The reference lists of the selected papers were checked for key papers. This systematic literature search was guided by PRISMA guidelines, which is preferred for reporting items for systematic reviews and meta-analyses developed by Cochrane Collaboration.19
Preferred Reporting Items for Systematic Reviews and Meta-Analyses flow chart. CINAHL, Cumulative Index of Nursing and Allied Health Literature; Embase, Excerpta Medica database; SSCI, The Social Sciences Citation Index.
Eligibility criteria
Studies eligible for inclusion met the following criteria: (1) included bereaved caregivers to patients diagnosed with HGG≥18 years, (2) described the caregiver’s perspective at post bereavement and (3) had been peer-reviewed prior to publication. Studies with different subtypes of PMBT were included only if findings were performed and extracted for the HGG population. Excluded were studies that included bereaved caregivers to patients under the age of 18 years and studies published before the year 2000. We limited the search to include studies published in Scandinavian language and/or English.
Data extraction and quality assessment
Information on the population (sample size and demographic data), study design (focus and time of enrolment) and main results was extracted and discussed within the reviewer team (KP, SN, MJ). The quality of the eligible studies was assessed using the Critical Appraisal Skills Programme,20 which comprises 10 individually scored items, assigned a plus sign when the criteria were clearly met, a minus sign when they were not and a combination of the two when information on how the criteria were addressed was unclear or lacking.
Results
The search resulted in the following: PubMed (n=144), CINAHL (n=107), Embase (n=419), SSCI (n=81), Scopus (n=268) and PsycINFO (n=83). There were 552 duplicates identified, resulting in 550 unique titles that, in addition to their abstracts, were reviewed by KP and SN, leading to the exclusion of 536 papers. These were excluded as they either included paediatric study participants, non-malignant brain tumours or merely were published as conference abstracts. Out of the 14 papers that appeared relevant for inclusion, 10 were excluded following full-text reading. Four qualitative studies were included in this review to provide insight into how bereaved caregivers of patients with HGG experience and manage their life situation after the death of the patient21–24 (figure 1) . Some studies included results representing both the period during the disease and after the patient had died. In these cases, only the results from the time at bereavement were extracted. Reasons for exclusion of two publications following full -text review were that they included bereaved caregivers were taken care of25 26 patients diagnosed with either an HGG or a low-grade tumour, and results were not outlined according to diagnosis. Four papers were excluded as the aim of these studies focused on the bereaved caregivers’ experience with the treatment trajectory9 27 28 or focused on EOL.29
Study design
The four included studies, published between 2004 and 2015, applied qualitative study designs with either participant interviews22–24 or a questionnaire survey with one open-ended response.21 One study included both patients and caregivers22 while three included caregivers only.21 23 24 The four studies included 105 caregivers, 62 of whom were bereaved. Findings were presented in the studies supported by participant quotations related to being a caregiver during the HGG disease and treatment trajectory and during the postbereavement period. In the following, each study design is presented chronologically based on year of publication (see online supplementary material).
Supplementary file 1
In the first article, Sherwood et al21 explored aspects of providing care for someone with HGG using a qualitative approach. Inclusion criteria were caregivers ≥21 years of age who had cared for someone also ≥21 years of age who had died of HGG. Sixty-two bereaved caregivers agreed to participate and were recruited from two national brain tumour support groups and an internet support group for bereaved caregivers. With a response rate of 69.4% (n=43), bereaved caregivers completed an anonymous self-reported questionnaire with one open-ended question and a questionnaire on socio-demographic data. The narrative responses ranged from two sentences to six pages, and content analysis was used to examine this qualitative dataset.
In the second article, Cavers et al22 aimed to understand factors influencing the process of adjustment to a diagnosis of glioma from before the diagnosis and until post bereavement. This qualitative study included 26 patients and 23 caregivers, recruited at a UK regional neurosurgical department representing a range of age, sex, tumour types and symptom profiles. Study participants participated in 80 in-depth qualitative interviews, 50% of which were carried out as joint interviews with patients and current caregivers. An overview of the interviews illustrated the time and reason for participant drop-out. The interviews were conducted at five key stages: (1) after surgery but before diagnosis (13 patients, 10 caregivers); (2) at start of oncology treatments (18 patients, 14 caregivers); (3) after completing treatment (15 patients, 10 caregivers); (4) 6 months after finalising the treatment plan (11 patients, seven caregivers) and (5) at post bereavement (conducted with nine caregivers no sooner than 3 months after the patient’s death). Interview transcripts were analysed using a constructionist grounded theory approach and cross-case analysis.
In the third article, Collins et al23 published a qualitative interview study (as part of a larger project) that provided an in-depth exploration of the needs and concerns of relatives caring for patients with HGG. The study focused on providing insight into bereaved family members’ experiences of caregiving. Participants (n=23) were recruited consecutively with a supplementary purposive sampling to ensure representation across a number of variables, including length of providing caring, stage of treatment, distance from hospital and type of care provision. Fifteen caregivers were approached to participate via patients from two Australian metropolitan hospitals, and eight bereaved caregivers were identified from a patient registry for palliative and oncology inpatient units. A recruitment flow chart illustrated the time and reason for participant drop-out. In-depth semistructured interviews with a predefined interview guide were used to collect data, which was examined using a thematic analysis based on grounded theory.
In the fourth article, Coolbrandt et al24 explored family caregivers’ experiences concerning the diagnosis, treatment, living with and caring for patients with HGG, as well as the caregivers’ needs. Seventeen caregivers were recruited from an oncology ward at University Hospital Leuven, Belgium (one caregiver withdrew). Sixteen caregivers participated in semistructured interviews. The interview guide was based on evidence from a systematic review of the experiences and needs of patients with HGG and their family caregivers.30 Four caregivers were invited to a follow-up interview on their experiences after the patients had died. Applying a grounded theory approach, data were analysed based on the Qualitative Analysis Guide of Leuven.31
Study participants
In the included studies (n=4), 105 people participated, 62 of whom were bereaved caregivers, providing the basis for this review on how caregivers of patients with HGG experience and manage their life situation after the patient’s death. A majority of the bereaved caregivers were female, HGG and spouses to the patient (n=76). Sample size in the studies ranged from 16 to 43 caregivers, of whom 2–43 were bereaved caregivers. The age of the caregivers was not listed in two of the studies, but ranged from 27 to 77 years in the two other studies.23 24 The most common diagnosis among the patients was GBM (n=87). Table 1 presents medical and demographic data.
Demographic data on study participants (n=105)
Perspectives on the caregiving role
Coolbrandt et al24 described how caregivers had been committed and determined to carry out the caregiver role. Reflecting back on the caregiver period at post bereavement, they were pleased that they had been able to provide care.24 However, bereaved caregivers also expressed a sadness caused by missed opportunities for sharing meaningful goodbyes, which they had expected at the time of their partner’s impending death. This was a challenge, however, due to the rapid deterioration of the patient’s cognitive ability.23 After the patient died, the caregivers were left with thoughts, regrets and unanswered questions. Some caregivers used coping strategies such as disavowal, both prior to and after death.22 Collins et al described how bereaved caregivers ruminated over regrets about care, particularly when the patient died at the hospital, instead of being able to meet the wishes of the patient to die at home.23 At post bereavement, some caregivers still felt distressed by unanswered questions about the patient’s disease and the cognitive and behavioural changes of the patient.23
Perspectives on the postbereavement period
Coolbrandt et al24 described how caregivers expressed an unmet need for support from professionals at post bereavement. The authors found that the caregivers needed to share concerns with the professionals and to discuss situations that were perceived as difficult. Bereaved caregivers appreciated supportive conversations or acknowledgement of their caregiving role, their feelings of burden and existing grief. Coolbrandt et al24 identified that there was a profound supportive care need after the patient’s death.
As Collins et al show,23 caregivers are also affected by physical symptoms and emotional reactions. Bereaved caregivers openly expressed the feelings of inadequacy related to the caring role due to the tremendous burden they experienced while the patient was alive. Bereaved caregivers’ physical health was negatively affected post bereavement and described feeling grief for a lengthy period of time after the patient’s death while trying to manage their loss.23 Sherwood et al21 described how bereaved caregivers found that the transition from being an active caregiver to a grieving caregiver was particularly difficult. Bereaved caregivers described the postbereavement situation as being negatively affected by feelings of exhaustion that arose during the period of caring. Suddenly they had time to themselves, which contrasted sharply with the period of giving care that is devoted almost entirely to caring for the patient. Sherwood et al also found that caregiver reactions to providing care did not end after the patients had deceased.21 Three studies reported that the bereaved caregivers had lost their social network while the patient was ill.21 23 24 In these cases, bereaved caregivers expressed a feeling of anger that contributed to their emotional strain after the patient had died.21
Methodological quality of the studies
This systematic review is based on four studies, three of which conducted interviews with the caregivers22–24 and one which applied a questionnaire survey with one open-ended response.21 Three studies collected data from both current and bereaved caregivers,22–24 while the remaining study only interviewed bereaved caregivers.21 The quality of each study is presented in table 2. Quality levels were to some extent similar between all four studies. The most common criticism across the studies was lack of reporting the relationship between the researcher and the participants. None of the four studies critically examined the researcher’s role and influence. All studies used appropriate qualitative and/or quantitative methods to address the research questions. Some studies, however, presented inadequate and, to some degree, less-than-detailed demographic data on participants, for example, failed to list the age of the patients. All of the studies defined participant inclusion and exclusion criteria for participants, although how precisely the criteria were defined varied. Sherwood et al21 merely presented an age criteria (>21 years) and the fact that the bereaved caregiver had cared for a patient with HGG. Cavers et al22 and Collins et al23 included participants who represented a variety of experiences, for example, time for caring, symptom profiles, type of care provision and background. Coolbrandt et al,24 in contrast, collected data using purposive sampling, superseded by theoretical sampling to confirm, deepen or refute concepts developed during the analysis. Three studies recruited participants through hospitals,22–24 while Sherwood et al21 recruited from support groups and an internet support group for bereaved caregivers. This difference can add to selection bias as the studies may represent participants experiencing either a greater challenge than the majority of participants who have the resources to seek a support group and thus represent a homogeneous group.21 Coolbrandt et al.,24 Sherwood et al21 and Collins et al23 recruited participants until data saturation was reached, benefiting internal validity.
Methodological quality of the studies
There is a risk of recall bias in the four studies due to the time that elapsed since the patients died and the time of the interviews or questionnaires. Cavers et al22 had a risk of recall bias as they were conducting their interviews with the bereaved relatives 3 months from bereavement and beyond that time. Collins et al23 carried out the interviews from 6 months to 3 years after. Sherwood et al21 and Coolbrandt et al24 did not report the period of time that had elapsed.
Discussion
This systematic review identified only four studies examining how caregivers of patients with HGG experience and manage their life situation after the patient’s death. The studies explored the bereaved caregivers’ experiences with similar designs, using various qualitative and quantitative (survey) methodological approaches to investigate their research questions. Bereaved caregivers expressed profound grief and had unmet questions related to the trajectory and their caring role. They were challenged by fatigue, emotional distress (sadness/depressive thoughts) and eventually a reduced work capacity and social network. Existing evidence suggests that caregivers may be at increased risk of developing depression. There is a correlation between caregivers’ depressive symptoms and behavioural challenges in the patient, such as hallucinations and agitation, factors proven to increase the risk of depression among caregivers.15 A long and difficult grieving process for bereaved caregivers of patients with HGG may reflect their need for psychological support. A longitudinal study conducted by Petruzzi et al26 described the changes in quality of life, including level of depression, experienced among caregivers of patients with mixed diagnosis of brain tumours during the disease trajectory and at 18 months post bereavement. However, Petruzzi et al identified an improvement the quality of life of caregivers, as measured during the treatment trajectory and compared with 18 months after the patient’s death.
The grieving process
The Diagnostic Statistical Manual of Mental Disorders32 states that the normal grieving process generally ends within 6 months after a loss. To identify if a normal grief process turns out to be complicated, Guldin et al33 developed a clinical tool to identify if bereaved caregivers suffer from complicated grief. However, feelings of grief must also be understood within a cultural context. Another tool is Beck’s Depression Inventory, which is a well-validated screening tool used to facilitate detection of complicated grief.33 Seen in light of our results and the identified grief during the early stages of caregiving to cognitively impaired family members,34 we recommend that caregivers are informed by the clinical specialist about the initial, normal or complicated grieving process. This way the bereaved caregivers will know when to seek support if the grieving process becomes prolonged and complicated. Screening allows early identification of depressive symptoms, leading to the timely launching of targeted initiatives and support designed to shorten and ease the grieving process for bereaved caregivers.
The Dual Process Model of coping with bereavement
To understand the grieving process, Stroebe and Schut35 developed the Dual Process Model of coping with bereavement, which identifies two categories of bereavement stressors, one that is loss-orientated and the other restoration-oriented. The loss-orientated stressor refers to concentrating on and dealing with the processing of some aspects of the loss experienced. Typically, this aspect involves ruminating about the deceased, about their life together and about the circumstances and events surrounding the death. The restoration-oriented stressor focuses on the caregivers’ needs and how they are dealt with. In other words, this aspect relates to the changes that are secondary consequences of the loss. The central component of Stroebe and Schut’s model is the dynamic, regulatory coping process of oscillation. According to the model, the grieving caregiver needs to both be confronted and to avoid the difficult tasks of grieving. This is in accordance with the results in the present review identifying that bereaved caregivers may need to follow a disavowal coping strategy.
Stroebe and Schut36 expanded the Dual Process Model with a family level to cover factors that affect the family domain. As a result, coping integrates loss-orientated and restoration-oriented tasks at both the individual and family levels. The loss-orientated family level relates to coming to terms with the death of the loved one. This process is highly relevant for bereaved caregivers of patients with HGG, who expressed thoughts, regrets and unanswered questions at post bereavement. The restoration-oriented family level relates to subjective and objective changes within the surrounding environment, that is, those brought about as a result of the death.36 This is expressed, for example, at post bereavement, where several bereaved caregivers of patients with HGG reported a loss of their social network during the time of the patient’s disease. In order to accommodate the bereaved caregiver in the grieving process, the Dual Process Model can play a relevant role in clinical practice, with the model furnishing important knowledge for clinical specialists to provide the necessary understanding and support for bereaved caregivers. An awareness of the oscillation process can lead to a new understanding of coping with the grieving process.
Study limitations
The literature review has some limitations. First, it only identified few studies (n=4), which means only limited knowledge is available to address the aim of this review. Second, the data in the studies used were collected at different time points, which makes it difficult to compare them directly. The study of Sherwood et al21 was published before the implementation of Stupp Regime,1 which could directly affect the caregivers’ perspectives, for example, as the patients’ prognosis improved (survival rate increased). This review nevertheless presents a sizeable population of bereaved caregivers (n=62). A total of 62 bereaved caregivers provided insight into the postbereavement period, but they represent a relatively small sample size for addressing the aims of this review.
Moreover, this review did not seek to address a specific point in time at post bereavement.
Clinical implications
This review sheds light on the bereaved caregiver’s concerns and unmet needs. Based on the experience of 62 bereaved caregivers, we suggest that a systematic approach is considered to be part of holistic need assessment to meet the needs of bereaved caregivers. Caregivers often experience feelings of grief at times when patients are impaired by cognitive a deficit, which often is detected at an early stage of the disease. We therefore recommend integrating information about the normal grieving process early in the disease trajectory. This information should include knowledge on how to distinguish normal sad feelings from signs of being depressed or experiencing complicated grief. Establishment of collaboration across sectors is necessary to identify and address the bereaved individual suffering from complicated grief. As an example, several countries have established National Centers for Grief where health professionals can refer grieving children, teens, young adults and their families to specialised counselling and treatment provided by psychologists.
Bereaved caregivers to patients with brain cancer are among the highest percentage ofjavascript:void(0); caregivers using bereavement services,37 and inspiration can be found in a caregiver programme in neuro-oncology,38 for example, through educational manuals on progressive disease and EOL information for the caregivers. Finally, a screening of those who are able to cope with understandable sadness versus those facing a complicated grieving process would indicate who is in the greatest need of being referred to specialised counselling.
Conclusion
In conclusion, bereaved caregivers have various unmet needs and preferences regarding the wish to discuss the disease trajectory and the care they provided with healthcare professionals. Moreover, the included studies revealed that caregivers may experience physical and emotional symptoms at post bereavement and a need to strengthen their social network. The review identified a gap in existing literature on how caregivers of patients with HGG experience or manage their life situation after the patient’s death. Hence, recommendations for best practice are not yet available and further research, including interventional studies, for bereaved caregivers of patients with HGG is required.
References
Footnotes
Contributors KP and SN contributed to the design and drafting of the manuscript. AL conducted the literature search together with KP and SN. SN, AL and MJ contributed to the conception and design and provided substantial scientific contribution and critical revision of important intellectual content. All authors have reviewed the manuscript critically and approved the final manuscript.
Funding This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.
Competing interests None declared.
Ethics approval This research did not involve human participants. Hence ethical approval was not required.
Provenance and peer review Not commissioned; externally peer reviewed.