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Abstract

Background:

The last three months of life (end-of-life phase) are profoundly challenging for patients with brain tumours and their family caregivers. Post-bereavement outcomes are largely unknown.

Aim:

To better understand long-term outcomes of a brain tumour diagnosis on families, we aimed to describe caregiver experiences during the end-of-life phase and beyond.

Design:

In this sequential mixed-methods study designed together with bereaved caregivers, we used an online survey. This comprised end-of-life experiences, and post-bereavement outcomes (family functioning: Family APGAR; resilience: CD-RISC-10; mood: HADS; prolonged grief: PG-13-R; post-traumatic stress: TSQ).

Setting/Participants:

Caregivers of patients with brain tumours who were bereaved ⩾6 months ago were invited through social media and charities.

Results:

105 bereaved neuro-oncology caregivers participated. The end-of-life phase was marked by high symptom burden and disruption to family life, compounded by often unsatisfactory information provision and support. Forty-three percent did not describe the patient’s death as dignified. Most caregivers were not well-supported post-bereavement, and current functioning was impacted by notable rates of prolonged grief disorder (64%), post-traumatic stress disorder (42%), depression (35%), anxiety (61%), disruption to family life (53%) and low levels of resilience. Multivariable regressions found better resilience and family functioning to be protective factors for both post-traumatic stress disorder and prolonged grief disorder symptoms, with a dignified death additionally linked to caregivers’ prolonged grief scores, explaining 23.8% and 51.0% of variance, respectively.

Conclusions:

Bereaved neuro-oncology caregivers have high rates of adverse mental health outcomes, highlighting a pressing need for improvements in palliative, end-of-life and post-bereavement services.

Keywords

Brain neoplasms palliative care death caregivers bereavement

What is already known about the topic?

Brain tumours diagnosed in adults can and often do lead to death;

Symptom burden is high throughout the disease trajectory and increases during the end-of-life phase, defined as the final 3 months.

What this paper adds

Bereaved caregivers often report unsatisfactory information provision and support in the end-of-life phase;

Long-term adverse outcomes include high rates of prolonged grief disorder (64%), post-traumatic stress disorder (42%), depression (35%), anxiety (61%), disruption to family life (53%) and low levels of resilience;

Better resilience and family functioning are protective factors for post-traumatic stress disorder and prolonged grief disorder.

Implications for practice, theory or policy

Patients with brain tumours and their caregivers both have profound palliative and end-of-life care needs which should be addressed;

Caregivers additionally require support into the post-bereavement phase to limit severe and long-lasting mental health and family life outcomes.

Introduction

Primary brain tumours can be classed as non-malignant or malignant, with a combined annual age-adjusted incidence rate of 24.25/100,000 (non-malignant 17.18/100,000; malignant: 7.06/100,000;).¹ Non-malignant brain tumours are typically less aggressive, however, depending on the location and treatment response, these can still result in significant disease burden^2,3 and ultimately may lead to death.⁴ Malignant, high-grade gliomas in particular are associated with a disproportionate share of cancer morbidity and mortality.⁵ These aggressive tumours can rapidly progress to the end-of-life phase,^5,6 defined as the last 3 months of life.^7,8

During the trajectory, symptom burden which includes oncological and neurological issues tends to increase over time, impacting on both patients’ and their families’ quality-of-life.^5,9
–11 Family caregivers consistently report high burden and unmet support needs,^12,13 which can extend into the end-of-life and post-bereavement period.^14
–17 The neurological deterioration makes the neuro-oncology end-of-life experience different to other cancers,⁵ with a higher frequency of disease-specific symptoms shortly before death.¹⁸ In the end-of-life phase, family caregivers can feel particularly unprepared and unsupported as patients experience, for example, loss of consciousness, difficulty swallowing, incontinence, seizures, progressive neurological and cognitive deficits, and headaches.^14,18,19 Still, specialist palliative care remains underutilized with between 57% and 80% of brain tumour patients not receiving services.^20,21 Indeed, among advanced cancer patients, those diagnosed with brain tumours are least likely to receive palliative care.²² Following the patient’s death, transitioning from providing care to being bereaved can be difficult.¹⁶ Whilst very little is known on post-bereavement outcomes of neuro-oncology caregivers,²³ a small-scale study noted high levels of distress.¹⁵ From research performed predominantly in other populations, we know caregivers are at risk for long-lasting negative impact on physical health, finances, family dynamics and relationships.^24
–28 In non-central nervous system cancer, better end-of-life experiences and quality of death have been linked to better caregiver quality-of-life post-bereavement.²⁹

Most published evidence is not specific to neuro-oncology, yet this population often has adverse outcomes compared to other oncological groups. We therefore aimed to describe the end-of-life experiences of brain tumour patients, as observed by their caregivers, and explore the longer-term impact on bereaved neuro-oncology caregivers. This work, co-designed and co-delivered by bereaved caregivers (PB and RM), will help highlight areas for improvement in palliative and end-of-life care, and post-bereavement support.

Methods

This report is part of a sequential mixed-methods study, comprising a quantitative survey followed by focus groups. Here, we report on the survey. The University of Leeds School of Medicine Research Ethics Committee provided approval (MREC 23-002).

Participants and procedures

Adult bereaved caregivers of brain tumour patients were invited to complete an online survey. Caregivers were eligible if they: had been bereaved for ⩾6 months; lived in the United Kingdom; had sufficient mastery of English to complete study procedures; had internet access and were able to provide consent. Caregivers were recruited from a closed Facebook group (‘Bereaved by a brain tumour’) which had ~1500 members and through charities’ (brainstrust and the Brain Tumour Charity) social media channels and/or newsletters. All participants confirmed consent and following survey completion, participants were offered a £10 voucher.

Outcome measures

Guided by caregiver representatives (PB and RM), outcome measures were selected which were deemed not too burdensome, taking ~60 min to complete. Self-reported basic sociodemographic and clinical information was collected alongside:

End-of-Life experiences: End-of-life Phase of Patients with a Malignant Brain Tumour Questionnaire.³⁰ This tool has adequate psychometric properties (content validity, internal consistency) and covers the last 3 months and last week of life. Questions focus on how caregivers thought the patient would have responded (38 items), and on caregivers’ own experiences during and following the end-of-life phase (21 items). Some items were modified to reflect the UK healthcare context.

Family functioning: Family APGAR.^31,32 This 5-item scale with adequate psychometric properties³³ yields a total score ranging from 0 to 10 with higher scores indicating better family functionality. Cut-off scores can discriminate between severely (0–3 points) and moderately dysfunctional families (4–6 points) and functional families (7–10 points).

Resilience: Connor-Davidson Resilience Scale-10 (CD-RISC-10).³⁴ This scale has good psychometric properties (construct validity, internal consistency) and includes 10 statements describing aspects of resilience scored on a 5-point scale (0–4). The total score ranges from 0 to 40, with higher scores indicative of greater resilience.

Anxiety and depression: Hospital Anxiety and Depression Scale (HADS).^35,36 HADS has adequate psychometric properties in caregiver studies (internal consistency).^37,38 In 14 items, scored on a 4-point scale (0-3), anxiety and depression are assessed. Clinically relevant cut-off scores exist for mild (0–7), moderate (8–10) and severe (11-21) symptoms of anxiety or depression.

Prolonged grief: Prolonged Grief Disorder-Revised (PG-13-R). This 13-item measure has excellent psychometric properties (internal consistency, test-retest reliability, discriminatory ability)³⁹ and maps onto the DSM-5-TR diagnostic criteria for prolonged grief disorder. A summary score ⩾30 is used to indicate the need for further evaluation and treatment of prolonged grief disorder.⁴⁰

Posttraumatic stress: the Trauma Screening Questionnaire (TSQ).⁴¹ The 10-item screening instrument is a valid tool with good sensitivity and specificity^42,43 and consists of five re-experiencing and five arousal items from the DSM-5 criteria for post-traumatic stress disorder. The optimal cut-off score for high risk of post-traumatic stress disorder is ⩾6.

Life events: the Life Events Checklist for DSM-5 (LEC5-standard).⁴⁴ This measure has good cross-cultural validity and reliability^45,46 and covers 16 events known to be highly distressing and/or associated with post-traumatic stress disorder, plus one additional item assessing any other extraordinarily stressful event.

Data analysis

Data were analysed using SPSS v.28. The sample’s sociodemographic and clinical characteristics were analysed descriptively. Questionnaires were scored along the respective scoring manuals and/or established criteria for clinically relevant cut-off scores. Descriptive statistics were generated to describe the end-of-life experiences (i.e. symptoms, support, quality-of-care, quality-of-life, quality-of-death) and caregivers’ initial post-bereavement outcomes. Current caregiver functioning was described using the scale scores, total scores, and clinically relevant cut-offs of the APGAR (family functioning), CD-RISC-10 (resilience), HADS (anxiety, depression), PG-13 (prolonged grief) and TSQ (post-traumatic stress). Life events were described using the LEC-5, with responses dichotomized to indicate whether caregivers had experienced a highly distressing life event (happened to them, witnessed it, learned about it, part of their job: yes) or not (not sure, doesn’t apply, do not want to answer: no), with a total score calculated to reflect the number of life events experienced.

Univariable regression analyses were done to explore potential factors associated with poor caregiver outcomes. For high risk of post-traumatic stress disorder (TSQ ⩾ 6) we explored associations with time since bereavement (<2 years or ⩾2 years), patient survival time (<18 months or ⩾18 months), patient age at death (<50 years or ⩾50 years), relationship (partner or other), stressful life events (LEC-5 excluding the items linked to illness, severe human suffering and ‘other’ as these could directly capturing the experience of caring for a brain tumour patient),⁴⁷ resilience (CD-RISC-10 total score),^48,49 family functioning (APGAR total score),⁵⁰ patient quality-of-life in the last 3 months (scale 1–7),⁵¹ dignified death (yes/no),⁴⁸ quality of care in the last 3 months (scale 1–7) and last week of life (scale 1–7),⁴⁸ and whether caregivers reported having had sufficient support in the end-of-life phase (yes/no).⁴⁸ Secondly, we ran univariable models to explore associations with prolonged grief in the subset of caregivers who were >12 months post-bereavement aligning with DSM criteria (symptoms present for ⩾1 year⁵²): univariable regression analyses with time since bereavement (<4 years or ⩾4 years), patient survival time (<18 months or ⩾18 months), patient age at death (<50 years or ⩾50 years), relationship (partner or other), resilience (CD-RISC-10 total score),⁵³ family functioning (APGAR total score),⁵⁴ patient quality-of-life in the last 3 months (scale 1–7),⁵¹ dignified death (yes/no),⁵⁵ quality-of-care in the last 3 months and last week of life (scale 1–7),^55,56 and whether caregivers reported having had sufficient support in the end-of-life phase (yes/no).⁵⁷ Those variables associated with post-traumatic stress disorder and prolonged grief disorder at p < 0.20 were taken forward into multivariable logistic regression models, where a manual backward selection was used to find the model with best fit (fewest number of variables, most variance explained using Nagelkerke R², examining model χ², p-values and Hosmer and Lemeshow tests).

Results

In total, 105 bereaved caregivers completed the survey between March and June 2024, see Table 1 for sociodemographic information and Supplementary Table 1 for participants’ religious/spiritual beliefs. Over half of our sample (N = 54, 51.4%) had an annual household income below £30,000, which is below the average UK household (median £32,400).⁵⁸

Table 1.

Caregiver and patient sociodemographic and clinical details.

Variables	n	%
Caregivers’ gender
Male	10	9.5
Female	95	90.5
Caregiver age^a
18–40	11	10.6
41–60	44	42.3
61–80	49	47.1
Caregivers’ ethnicity^a
Asian or Asian British^c	1	0.9
Dual heritage^d	1	0.9
White^e	102	97.1
Caregivers’ highest level of education attained
None	1	0.9
Secondary	16	15.2
Further education (sixth form/college)	34	32.4
Higher education	32	30.5
Vocational qualification	1	0.9
Postgraduate	21	20.0
Caregivers’ employment status
Full time (⩾30 h)	25	23.8
Part time (<30 h)	20	19.0
Self-employed	6	5.7
Student	2	1.9
Caring for family/home	2	1.9
Unemployed but looking for work	3	2.9
Unable to work due to illness/disability	5	4.8
Retired	42	40
Annual household income^b
Less than £10,000	8	7.6
£10,000–£19,999	27	25.7
£20,000–£29,999	19	18.1
£30,000–£39,999	8	7.6
£40,000–£49,999	3	2.9
£50,000–£59,999	4	3.8
£60,000–£69,999	3	2.9
£70,000–£79,999	3	2.9
£80,000–£89,999	1	1.0
£90,000–£99,999	1	1.0
>£100,000	6	5.7
Prefer not to say	20	19.0
Country in the UK^b
England	93	88.6
Northern Ireland	2	1.9
Scotland	5	4.8
Wales	3	2.9
Caregiver relationship to patient
Partner of patient	76	72.4
Parent of patient	10	9.5
Child of patient	19	18.1
Intensity of contact with patient in last 3 months
Lived together	84	80.0
In touch daily	20	19.0
Restricted due to Covid-19	1	1.0
Residence 3 months before death
At home	92	87.6
In a nursing home	2	1.9
In a hospital	8	7.6
In a hospice	1	1.0
Other	2	1.9
Age of patient when died
18–40	12	11.4
41–60	45	42.9
61–80	46	43.8
81–90	2	1.9
Patients’ highest level of education attained
None	1	0.9
Secondary	24	22.9
Further education (sixth form/college)	41	39.0
Higher education (university undergraduate)	20	19.0
University postgraduate	16	15.2
Other (e.g. chartered/professional award)	3	2.9
Type of brain tumour
Glioma	95	90.5
Meningioma	1	0.9
Other^f	6	5.7
Don’t know	3	2.9
Tumour grade (WHO)
Grade I	1	0.9
Grade II	3	2.9
Grade III	3	2.9
Grade IV	88	83.8
Don’t know	10	9.5
How long did the patient live with this diagnosis
Less than 6 months	28	26.7
6 months to 1 year	24	22.9
1 year to 18 months	15	14.3
19 months to 2 years	16	15.2
2–5 years	14	13.3
More than 5 years	8	7.6
Time since bereavement
6 months to 1 year	24	22.9
1–1.5 years	18	17.1
1.5–2 years	11	10.5
2–3 years	11	10.5
3–4 years	7	6.7
4–5 years	10	9.5
5–10 years	17	16.2
Over 10 years	7	6.7

1 missing.

2 missing.

Indian n = 1.

White and Black African n = 2.

British n = 52; English n = 35; Irish n = 2; Scottish n = 8; Welsh n = 1; Other White background n = 4.

Other = Hemangiopericytoma; Malignant melanoma; Medulloblastoma; Pineoblastoma; Primary CNS Lymphoma; Brain metastases.

End-of-life experiences

Symptoms and family functioning

Patients’ end-of-life symptoms are displayed in Figure 1 and Supplementary Figure 1 shows the frequency of epileptic seizures.¹¹ Thirty-two caregivers (31.1%) reported other symptoms reported as free text responses most frequently sight problems (N = 6, 5.7%), confusion (N = 5, 4.8%) and behaviour changes (N = 5, 4.8%).

Figure 1.

Symptoms in the last 3 months (panel A) and last week of life (panel B) as reported by the caregiver.

Social activities were nearly always impacted (quite a bit or very much: N = 93, 88.6% in the last 3 months; N = 84, 80.0% in the last week of life for patients; N = 102, 97.1% in the final 3 months for caregivers). Caregivers commonly reported severe (N = 81, 77.1%) or moderate (N = 16, 15.2%) disruption to family life. The relationship between caregiver and patient often became disrupted (N = 40, 38.1%) or more intense (N = 46, 43.8%). Caregivers’ work ability was often impacted (N = 77, 73.3%). Nearly half reported disease-related financial difficulties (a little to very much: N = 49, 46.7%).

Quality of care and quality-of-life

About half of caregivers found the quantity of information provided about the illness insufficient (N = 53, 50.5%). Caregivers often did not receive the professional support they needed in the last 3 months, with 46 receiving some, but not enough support (43.8%) and 18 receiving no support at all (17.1%). Supplementary Table 2 displays the healthcare workers encountered during the disease.

Quality of care in the last 3 months before death was rated average (M = 3.97, SD = 1.69, scale 1 to 7 (very poor-excellent). This was better during the last week of life (M = 4.82, SD = 1.94). In most cases, healthcare professionals involved in delivering care in the last week (see Table 2) explained end-of-life care options to either the patient (N = 6, 5.7%), the caregiver (N = 34, 32.4%), or both (N = 38, 36.2%). Most caregivers were satisfied with the contact with this professional (N = 60, 57.1%), their own role (N = 64, 61.0%) and with their involvement in decision-making (N = 67, 63.8%), although over a third felt insufficiently involved (N = 38, 36.2%). Healthcare professionals were not always accessible (sometimes accessible: N = 52, 49.5%; not accessible: N = 9, 8.5%). Over half of caregivers indicated that healthcare professionals should have played a larger role in patient care (N = 54, 51.4%).

Table 2.

End-of-life care.

Outcomes	N = 105
Quality of care M, SD^a
Scale 1–7 (very poor to excellent)
Last 3 months of life	3.97	1.69
Last week of life	4.82	1.94
Patient treatment preferences N, %
No preferences expressed	31	29.5%
Did not want any treatment	2	1.9%
Wanted only supportive treatment	13	12.4%
Some anti-tumour treatment, but not all	9	8.6%
Wanted all possible anti-tumour treatment	50	47.6%
Change in treatment preferences occurred before death N, %
Yes	9	8.6%
Healthcare professionals involved in care in last week N, %
Hospice doctors	38	36.2%
General practitioners	21	20.0%
Specialist doctors	14	13.3%
Nursing home doctors	3	2.9%
Other professionals:	29	27.6%
Allied health professionals	19	18.1%
Social workers	3	2.9%
Patient was able to decide on end-of-life care the week before death N, %
Yes	7	6.7%
Partly	14	13.3%
No	84	80.0%
Caregiver influence on end-of-life care the week before death N, %
No influence	16	15.2%
Little influence	18	17.1%
Extensive influence	66	62.9%
Not applicable	5	4.8%
Decisions made in end-of-life care contradictory to wishes N, %
Contradictory to patient wishes	8	7.6%
Contradictory to caregiver wishes	30	28.6%
Advanced written directive N, %^b
Yes	20	19.0%
No	83	79.0%
Transfers (any moves or admissions) during the last 3 months N, %
Once	23	21.9%
Twice	9	8.6%
Three times	8	7.6%
Four times	8	7.6%
Five times	2	1.9%
Six times	1	1.0%
Timing of transfers N, %
In the last week	26	24.8%
In the last month	25	23.8%
In the last 3 months	17	16.2%
Patient interest in euthanasia N, %
If euthanasia were an option, patient would have wanted this	31	29.5%
Patient never expressed an opinion about euthanasia	25	23.8%
Patient did not want euthanasia	25	23.8%
Unknown	24	22.9%
Place of death N, %
At home	52	49.5%
Hospital	17	16.2%
Hospice	29	27.6%
Nursing home	4	3.8%
Other	3	2.8%
Place of death matched preference N, %
Yes	63	60.0%
No	32	30.5%
No preference expressed	10	9.5%

1 missing.

2 missing.

Caregivers’ proxy ratings of patient quality-of-life in the last 3 months before death, was poor (M = 2.13, SD = 1.46, scale from 1 to 7 (very poor-excellent)). They rated their own quality-of-life in the end-of-life phase similarly poor (M = 2.40, SD = 1.42). Most patients were aware of their imminent death either fully, or more-or-less (N = 72, 68.6%). Advance directives were made by N = 20 (19.0%) patients, wills were prepared or discussed by N = 46 (43.8%).

Quality of death

The death of the patient was described as dignified or very dignified by 60 caregivers (57.1%). However, 22 caregivers (20.9%) felt the death was neither dignified nor undignified, and 23 caregivers (21.9%) reported the death as undignified. Table 3 displays factors reported as influencing the dignity of death.

Table 3.

Reported reasons affecting dying with dignity.

Reason	N	%	Illustrative quote from free text responses, where available
Not being able to communicate	69	65.7	‘Everything that my husband loved and valued about life was taken from him by the disease. He fought bravely until the very end, but he was left almost in a vegetive state. No one could tell me what he was thinking/feeling/experiencing- and I couldn't by the end’.
Not being able to take care of oneself	64	60.9	‘Being doubly incontinent’.
Not being able to take care of oneself	64	60.9	‘There is absolutely no dignity in being blind unable to walk talk feed yourself’.
The feeling of losing control	60	57.1	‘Things like catheters, not being able to move etc. it was horrific’.
Not being able to think clearly	48	45.7
The feeling of becoming a burden to others	41	39.0	‘Dad really struggled with allowing anyone to look after him. He hated that he needed my help with using the bathroom and taking care of himself’.
Feeling of a loss of meaning of life	18	17.1	‘Aged 26 a [university] graduate [. . .], married for 9 short weeks. To watch your beautiful talented kind caring adult child reduced to a vegetable is heartbreaking’.
Not being able to accept the truth	16	15.2
Not being treated with respect	11	10.5
Free text responses of reasons not already covered above
Ineffective pain management	2	1.9	‘They couldn't get the painkilling meds at a level where he was very comfortable. He was in dreadful pain and in the end they had to use four syringe drivers and a rarely used extra painkiller from hospice doctor on top of the high doses of morphine so he could get relief. He was only unconscious last few days’.
Ineffective pain management	2	1.9	‘. . .Also in pain and nothing you can do to help just be there’.
The patient being unaware of dying	1	0.9	‘He was unaware he was in the last days of his life. He thought he was due to have surgery and then 6 months chemo/radio before surviving for 12-18 months’
COVID-related restrictions	1	0.9	‘Due to covid he was not allowed visitors, we were called to say he’d passed away, we never got to say goodbye, he died holding a strangers hand, a care assistant on her first shift, he would have hated that, he would have been embarrassed’.
Failed resuscitation attempts	1	0.9	‘I felt that my husband's last few hours were quite violent and brutal. He was a tall, well-built man and to get him off the bed onto the floor to attempt CPR I had to drag him by his ankles and it was heartbreaking. I was on my own and trying to do my best to resuscitate him. Then I witnessed the paramedics trying to resuscitate using everything they had. It was simply the worst night of my life and totally unexpected. At 9 pm he was eating steak and chips, by 1 am he was having a seizure and by 3 am he lost his battle’.

Immediate post-bereavement outcomes and support needs

Approximately half (N = 53, 50.5%) of caregivers felt insufficiently supported by friends and family following the patient’s death. About a third of caregivers were in contact with the patient’s healthcare professionals following the patient’s death (N = 31, 29.5%), but only 14 (13.3%) had been offered the opportunity to discuss end-of-life care after death. Over half of caregivers expressed needing professional help after the patient’s death (N = 54, 51.4%), but only 11 received as much help as they needed (10.5%), with 30 receiving some help (28.6%), and 13 receiving no help (12.4%).

Current functioning of bereaved caregivers

Caregivers had been bereaved for a median of 1.5 to 2 years (range: 6 months to 10+ years) (see Table 1). Caregivers rated their current quality-of-life as average (M = 3.93, SD = 1.57). Over a third of caregivers had severe symptoms of depression (HADS-D > 8, N = 37, 35.2%), and nearly two-thirds had severe symptoms of anxiety (HADS-A > 8, N = 64, 61.0%), see Table 4. Over half currently experienced disruption to family functioning (APGAR moderate/severe dysfunction, N = 56 (53.3%)). In general, resilience was low with M = 21.98 (SD = 9.24) on CD-RISC-10 (norm population M ≈ 32).³⁴ The majority (N = 82, 78.1%) had resilience scores falling within the lowest quartile of population-based norms.³⁴ Nearly all caregivers experienced ⩾1 symptom of post-traumatic stress disorder in the past week (N = 92, 87.6%), and 44 caregivers (41.9%) were at high risk for post-traumatic stress disorder (TSQ ⩾ 6).

Table 4.

Long-term outcomes of bereaved caregivers.

Outcomes	N = 105
Post-traumatic stress (TSQ)
Total score, M (SD), range^a	5.31 (2.99), 0–10
Below cut-off for PTSD N (%)	55 (52.4)
Above cut-off for PTSD N (%)	44 (41.9)
Prolonged grief (PG-13-R)
Full sample (N = 105) total score, M (SD), range	34.47 (10.04), 13–50
12+ months bereaved (N = 81) total score, M (SD), range	33.16 (10.23), 13–50
Full sample (N = 105) below cut-off for PGD N (%)	33 (31.4)
12+ months bereaved (N = 81) below cut-off for PGD N (%)	29 (35.8)
Full sample (N = 105) above cut-off for PGD N (%)	72 (68.6)
12+ months bereaved (N = 81) above cut-off for PGD N (%)	52 (64.2)
Resilience (CD-RISC-10)
M (SD)	21.98 (9.24)
Lowest quartile (population norms) N (%)	82 (78.1)
Second quartile (population norms) N (%)	7 (6.7)
Third quartile (population norms) N (%)	11 (10.5)
Highest quartile (population norms) N (%)	5 (4.8)
Depressive symptoms (HADS-D)
M (SD), range	9.07 (5.27), 0–21
Mild N (%)	37 (35.2)
Moderate N (%)	31 (29.5)
Severe N (%)	37 (35.2)
Anxiety (HADS-A)
M (SD), range	11.44 (4.80), 1–21
Mild N (%)	21 (20.0)
Moderate N (%)	20 (19.0)
Severe N (%)	64 (61.0)
Life events (LEC-5)
Total number of life events M (SD), range	4.93 (4.13), 0–17
Family functioning (Family APGAR)
Total score M (SD), range^b	6.09 (3.11), 0–10
Functional family N (%)	48 (45.7)
Moderately dysfunctional family N (%)	36 (34.3)
Severely dysfunctional family N (%)	20 (19.0)

Family APGAR: Family APGAR (adaptation, partnership, growth, affection and resolution); CD-RISC-10: Connor-Davidson Resilience Scale-10; HADS-A: Hospital Anxiety and Depression Scale-Anxiety; HADS-D: Hospital Anxiety and Depression Scale-Depression; LEC-5: Life Events Checklist for DSM-5; PG-13-R: Prolonged Grief Disorder-Revised; TSQ: Trauma Screening Questionnaire.

6 missing.

1 missing.

Univariable logistic regressions to explore potential predictors of risk for developing post-traumatic stress disorder are shown in Supplementary Table 3. The multivariable model which included resilience and family functioning was statistically significant χ²(2) = 19.192 p < 0.001, and explained 23.8% of the variance in post-traumatic stress (Nagelkerke R²). Better resilience (CD-RISC-10 total score) and family functioning (APGAR total score) was associated with a reduction in the likelihood of caregivers displaying post-traumatic stress disorder (B = −0.078, p = 0.005, OR = 0.925, 95% CI = 0.876 to 0.977, family functioning (B = −0.163, p = 0.079, OR = 0.849, 95% CI = 0.728 to 0.991).

81 respondents were ⩾12 months post-bereavement, see Figure 2. Of those, 64.2% (N = 52) had scores indicative of prolonged grief disorder (PG-13-R ⩾ 30). Univariable logistic regressions to explore potential predictors for caregivers’ risk of developing prolonged grief disorder are shown in Supplementary Table 3. The multivariable model including resilience and dying with dignity was statistically significant χ²(2) = 37.298 p < 0.001, and explained 51.0% of the variance in prolonged grief disorder (Nagelkerke R²). Better resilience as measured with CD-RISC-10 (B = −0.193, p < 0.001, OR = 0.824, 95% CI = 0.748–0.908), better family functioning (B = −0.181, p = 0.089, OR = 0.835, 95% CI = 0.678–1.028) and the patient dying with dignity (B = −2.031, p = 0.025, OR = 0.131, 95% CI = 0.022–0.771) were associated with a reduction in the likelihood of caregivers exhibiting prolonged grief disorder.

Figure 2.

The proportion of caregivers, at least 12 months since bereavement, who scored above the cutoff for prolonged grief disorder and/or post-traumatic stress disorder.

Discussion

Key findings

Our study covers experiences and long-term outcomes of 105 bereaved neuro-oncology caregivers, yielding five key results. First, caregivers report high patient symptom burden and disruption to family life in the end-of-life, with room for improvement in terms of quality of care around information, support and accessibility of healthcare professionals. Second, a significant proportion of bereaved caregivers (~43%) did not describe the death of the patient as dignified. Third, over half of caregivers did not feel well-supported following the death of the patient. Fourth, caregivers’ current functioning post bereavement was suboptimal with notable rates of depression (35%), anxiety (61%), disruption to family life (53%) and low levels of resilience. Fifth, 42% scored above the threshold for high risk of post-traumatic stress disorder and 64% of those who were at least a year post-bereavement scored above the threshold for high risk of prolonged grief disorder, both mental disorders according to DSM-V.

Post-traumatic stress and prolonged grief disorders

The rates for high risk of post-traumatic stress disorder found in our investigation (42%) are higher than those observed in bereaved caregivers of other terminal cancer patients (30%)⁵⁹ or neuro-intensive care unit patients (22%).⁶⁰ We found greater resilience and better family functioning to be protective factors for post-traumatic stress disorder, explaining 23.8% of variance. This indicates other factors are involved. Other studies found negative affectivity, social support, locus of control in relation to the loss,⁵⁹ time spent at the bedside and lower household income⁶⁰ linked to post-traumatic stress disorder. Post-traumatic stress disorder is also directly associated with prolonged grief disorder.⁶¹ In our sample, the rates of prolonged grief disorder were high at 64%, considering only 7% to 10% of adults typically develop prolonged grief issues.⁶² Other studies using self-report measures show prevalence rates of 5% to 22%.^60,63,64 Our findings contrast other evidence suggesting bereaved caregivers’ prolonged grief scores often return back to the levels of matched controls by 9 to 10 months follow-up.⁶⁵ In bereaved cancer caregivers, prolonged grief disorder can precede the development of major depressive disorder.⁶⁶ Indeed, 35% of our sample had scores indicative of high risk for depression. In our study, better caregiver resilience, family functioning and a dignified death were protective factors for prolonged grief disorder, explaining 51% of the variance, which is broadly in line with the literature. Other investigations additionally identified that pre-loss anticipatory grief, early prolonged grief symptoms, greater bereavement dependency, a spousal relationship to the patient, greater caregiver burden, poor family functioning, poor coping and low levels of optimism were risk factors for developing symptoms of prolonged grief disorder.^54,64

It is striking, though perhaps unsurprising given the low rates of timely specialist palliative care involvement,^20
–22 that our sample appears at higher risk for adverse outcomes post-bereavement than other caregiver populations. With its combination of neurological and oncological symptom burden, the often-rapid decline in patient functioning and high end-of-life symptom burden, the neuro-oncology caregiver experience can be described as combining the worst of cancer and dementia.⁶⁷ The focus groups performed in a nested sample of survey participants (manuscript in preparation) will shed further light on the potential reasons for adverse post-bereavement outcomes.

Guidelines exist for the management of post-traumatic stress disorder and prolonged grief disorder. For post-traumatic stress disorder, individual or group-based cognitive behavioural therapy with a trauma focus, and/or eye movement desensitization reprocessing is recommended by the World Health Organization and the National Institute for Health and Care Excellence.^68,69 For post-traumatic stress disorder, pharmacological treatment is not advised.^68,69 The National Institute for Health and Care Excellence does not have prolonged grief disorder guidelines and interestingly, the World Health Organization only recommends what not to do in people without prolonged grief disorder: interventions should not be offered routinely to all bereaved individuals.⁶⁸ However, benzodiazepines and grief counselling may be advised for those who do meet criteria for prolonged grief disorder as a mental disorder. With recent systematic reviews not identifying any trials of support interventions targeted at bereaved neuro-oncology caregivers,^70
–73 there is a need for future work.

Strengths and limitations

This investigation was designed and delivered together with bereaved caregivers. There is some recruitment bias from the Facebook group, possibly overestimating the prevalence of issues. We attempted to counter this by also recruiting through charities. The sample is predominantly made up of white, female spousal caregivers, which, although common in neuro-oncology caregiver studies, is a limitation in terms of diversity. Given the variable time since bereavement, recall bias for the end-of-life experiences cannot be ruled out. The cross-sectional nature of the study did not enable us to explore the development of risk factors for mental disorders over time. Strengths include the relatively large sample, and detailed assessment of both end-of-life experiences and post-bereavement outcomes. The qualitative findings from our focus groups will provide further explanatory value in a separate article.

Conclusions

Our work highlights significant and enduring vulnerabilities in bereaved neuro-oncology caregivers. Timely intervention is needed to prevent long-lasting adverse impacts of brain tumours on families, extending beyond the disease trajectory.

Supplemental Material

sj-docx-1-pmj-10.1177_02692163251344164 – Supplemental material for End-of-life care experiences and long-term outcomes of bereaved neuro-oncology caregivers: A cross-sectional survey

Supplemental material, sj-docx-1-pmj-10.1177_02692163251344164 for End-of-life care experiences and long-term outcomes of bereaved neuro-oncology caregivers: A cross-sectional survey by Shaista Meer, Peter Buckle, Rosanna Miller, Louise Murray, Lucy Ziegler, Karin Piil and Florien Boele in Palliative Medicine

Footnotes

Acknowledgements

We would like to thank all participants for their time and effort. We also thank brainstrust and the Brain Tumour Charity for supporting recruitment.

Authorship

Conceptualization: PB, RM, LM, LZ, KP, FB

Methodology: PB, RM, LM, LZ, KP, FB

Investigation: SM, PB, RM, FB

Data curation: SM, PB, RM

Formal analysis: SM, FB

Writing (original draft): SM, FB

Writing (review & editing): SM, PB, RM, LM, LZ, KP, FB

Resources: FB

Data availability

The data that support the findings of this study are available from the corresponding author (FB), upon reasonable request and following appropriate agreements.

Declaration of conflicting interests

The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: FB: speaker (Medscape, Medtalks, Servier); KP: consultancy (Servier), speaker (Medscape).

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: University of Leeds Academic Development Grant and Yorkshire Cancer Research (L389FB).

ORCID iDs

Rosanna Miller

Lucy Ziegler

Karin Piil

Florien Boele

Supplemental Material

Supplemental material for this article is available online.

References

Ostrom

Cioffi

Waite

, et al. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2014–2018. Neuro Oncol 2021; 23: iii1–iii105.

Zamanipoor Najafabadi

van der Meer

Boele

, et al. Determinants and predictors for the long-term disease burden of intracranial meningioma patients. J Neurooncol 2021; 151: 201–210.

Frances

Murray

Nicklin

, et al. Long-term health-related quality of life in meningioma survivors: a mixed-methods systematic review. Neuro-Oncol Adv 2024; 6: vdae007.

Holleczek

Zampella

Urbschat

, et al. Incidence, mortality and outcome of meningiomas: a population-based study from Germany. Cancer Epidemiol 2019; 62: 101562.

Sizoo

Pasman

HRW

Dirven

, et al. The end-of-life phase of high-grade glioma patients: a systematic review. Support Care Cancer 2014; 22: 847–857.

Schubart

Kinzie

Farace

. Caring for the brain tumor patient: family caregiver burden and unmet needs. Neuro Oncol 2008; 10: 61–72.

Foley

Carver

. Palliative care in neurology: an overview. Neurol Clin 2001; 19: 789–799.

Sepúlveda

Marlin

Yoshida

, et al. Palliative care: the World Health Organization’s global perspective. J Pain Symptom Manage 2002; 24: 91–96.

IJzerman-Korevaar

Snijders

de Graeff

, et al. Prevalence of symptoms in glioma patients throughout the disease trajectory: a systematic review. J Neurooncol 2018; 140: 485–496.

10.

Piil

Jakobsen

Christensen

, et al. Health-related quality of life in patients with high-grade gliomas: a quantitative longitudinal study. J Neurooncol 2015; 124: 185–195.

11.

Sizoo

Taphoorn

Uitdehaag

, et al. The end-of-life phase of high-grade glioma patients: dying with dignity? Oncologist 2013; 18: 198–203.

12.

Coolbrandt

Sterckx

Clement

, et al. Family caregivers of patients with a high-grade glioma: a qualitative study of their lived experience and needs related to professional care. Cancer Nurs 2015; 38: 406–413.

13.

Collins

Lethborg

Brand

, et al. The challenges and suffering of caring for people with primary malignant glioma: qualitative perspectives on improving current supportive and palliative care practices. BMJ Support Palliat Care 2014; 4: 68–76.

14.

Piil

Nordentoft

Larsen

Jarden

. Bereaved caregivers of patients with high-grade glioma: a systematic review. BMJ Support Palliat Care 2019; 9: 26–33.

15.

Lobb

Halkett

McDougall

, et al. Bereavement outcomes of carers of patients with high grade glioma: experiences of support before and after the death. Death Stud 2023; 47: 1094–1103.

16.

Sherwood

Given

Doorenbos

, et al. Forgotten voices: lessons from bereaved caregivers of persons with a brain tumour. Int J Palliat Nurs 2004; 10: 67–75.

17.

Piil

Jarden

. Bereaved caregivers to patients with high-grade glioma: a qualitative explorative study. J Neurosci Nurs 2018; 50: 94–99.

18.

Koekkoek

Dirven

Sizoo

, et al. Symptoms and medication management in the end of life phase of high-grade glioma patients. J Neurooncol 2014; 120: 589–595.

19.

Barbaro

Blinderman

Iwamoto

, et al. Causes of death and end-of-life care in patients with intracranial high-grade gliomas: a retrospective observational study. Neurology 2022; 98: e260–e266.

20.

Ozanne

Öhlén

Nyblom

, et al. Disparities in end-of-life care and place of death in people with malignant brain tumors: a Swedish registry study. Neuro Oncol Pract 2024: npae113.

21.

Nåhls

N-S

Anttonen

Nuutinen

, et al. The impact of palliative care contact on the use of hospital resources at the end of life for brain tumor patients; A nationwide register-based cohort study. J Neurooncol 2025; 172(3): 549–556.

22.

Bennett

Ziegler

Allsop

, et al. What determines duration of palliative care before death for patients with advanced disease? A retrospective cohort study of community and hospital palliative care provision in a large UK city. BMJ Open 2016; 6: e012576.

23.

Morris

Sannes

. Bereavement care for family caregivers of neuro-oncology patients. Ann Palliat Med 2021; 10: 95363.

24.

Adelman

Tmanova

Delgado

, et al. Caregiver burden: a clinical review. JAMA 2014; 311: 1052–1060.

25.

Sherwood

Price

Weimer

, et al. Neuro-oncology family caregivers are at risk for systemic inflammation. J Neurooncol 2016; 128: 109–118.

26.

Von Känel

Mausbach

Patterson

, et al. Increased Framingham Coronary Heart Disease Risk Score in dementia caregivers relative to non-caregiving controls. Gerontology 2008; 54: 131–137.

27.

Pinquart

Sörensen

. Correlates of physical health of informal caregivers: a meta-analysis. J Gerontol Ser B Psychol Sci Soc Sci 2007; 62: P126–P137.

28.

Stroebe

Schut

. Family matters in bereavement: toward an integrative intra-interpersonal coping model. Perspect Psychol Sci 2015; 10: 873–879.

29.

Garrido

Prigerson

. The end-of-life experience: modifiable predictors of caregivers' bereavement adjustment. Cancer 2014; 120: 918–925.

30.

Sizoo

Dirven

Reijneveld

, et al. Measuring health-related quality of life in high-grade glioma patients at the end of life using a proxy-reported retrospective questionnaire. J Neurooncol 2014; 116: 283–290.

31.

Smilkstein

. The family APGAR: a proposal for a family function test and its use by physicians. J Fam Pract 1978; 6: 1231–1239.

32.

Goodman

Hoven

Narrow

, et al. Measurement of risk for mental disorders and competence in a psychiatric epidemiologic community survey: the National Institute of Mental Health Methods for the Epidemiology of Child and Adolescent Mental Disorders (MECA) study. Soc Psychiatry Psychiatr Epidemiol 1998; 33: 162–173.

33.

Alfaro-Diaz

Esandi

Clausen

, et al. Instruments for assessing family functioning in adults patients with cancer: a systematic review of measurement properties. Semin Oncol Nurs 2024; 40: 151729.

34.

Campbell-Sills

Stein

. Psychometric analysis and refinement of the connor–davidson resilience scale (CD-RISC): validation of a 10-item measure of resilience. J Trauma Stress 2007; 20: 1019–1028.

35.

Zigmond

Snaith

. The hospital anxiety and depression scale. Acta Psychiatr Scand 1983; 67: 361–370.

36.

Spinhoven

Ormel

Sloekers

, et al. A validation study of the Hospital Anxiety and Depression Scale (HADS) in different groups of Dutch subjects. Psychol Med 1997; 27: 363–370.

37.

Gough

Hudson

. Psychometric properties of the Hospital Anxiety and Depression Scale in family caregivers of palliative care patients. J Pain Symptom Manage 2009; 37: 797–806.

38.

Lambert

Pallant

Girgis

. Rasch analysis of the hospital anxiety and depression scale among caregivers of cancer survivors: implications for its use in psycho-oncology. Psycho Oncol 2011; 20: 919–925.

39.

Prigerson

Boelen

, et al. Validation of the new DSM-5-TR criteria for prolonged grief disorder and the PG-13-Revised (PG-13-R) scale. World Psychiatry 2021; 20: 96–106.

40.

Prigerson

Shear

Reynolds

. Prolonged grief disorder diagnostic criteria—Helping those with maladaptive grief responses. JAMA Psychiatry 2022; 79: 277–278.

41.

Brewin

Rose

Andrews

, et al. Brief screening instrument for post-traumatic stress disorder. Br J Psychiatry 2002; 181: 158–162.

42.

Mouthaan

Sijbrandij

Reitsma

, et al. Comparing screening instruments to predict posttraumatic stress disorder. PLoS ONE 2014; 9: e97183.

43.

de Bont

van den Berg

van der Vleugel

, et al. Predictive validity of the Trauma Screening Questionnaire in detecting post-traumatic stress disorder in patients with psychotic disorders. Br J Psychiatry 2015; 206: 408–416.

44.

Weathers

Blake

Schnurr

, et al. The life events checklist for DSM-5 (LEC-5). 2013. Instrument available from the National Center for PTSD at www.ptsd.va.gov

45.

Tari

Wong

. Exploring the factor structure and psychometric properties of the Life Events Checklist (LEC-5) Scale in adolescent school children. Nature-Nurture Journal of Psychology 2024; v4i1.41. DOI: 10.53107/nnjp.v4i1.41

46.

Rzeszutek

Lis-Turlejska

Palich

, et al. The Polish adaptation of the Life Events Checklist (LEC-5) for PTSD criteria from DSM-5. Psychiatr Pol 2018; 52: 499–510.

47.

Lukaschek

Kruse

Emeny

, et al. Lifetime traumatic experiences and their impact on PTSD: a general population study. Soc Psychiatry Psychiatr Epidemiol 2013; 48: 525–532.

48.

Carmassi

Foghi

Dell’Oste

, et al. Risk and protective factors for PTSD in caregivers of adult patients with severe medical illnesses: a systematic review. Int J Environ Res Public Health 2020; 17: 5888.

49.

Horn

Charney

Feder

. Understanding resilience: new approaches for preventing and treating PTSD. Exp Neurol 2016; 284: 119–132.

50.

Evans

Cowlishaw

Forbes

, et al. Longitudinal analyses of family functioning in veterans and their partners across treatment. J Consult Clin Psychol 2010; 78: 611.

51.

Abbott

Prigerson

Maciejewski

. The influence of patients’ quality of life at the end of life on bereaved caregivers’ suicidal ideation. J Pain Symptom Manage 2014; 48: 459–464.

52.

Prigerson

Kakarala

Gang

, et al. History and status of prolonged grief disorder as a psychiatric diagnosis. Annu Rev Clin Psychol 2021; 17: 109–126.

53.

Mancini

Sinan

Bonanno

. Predictors of prolonged grief, resilience, and recovery among bereaved spouses. J Clin Psychol 2015; 71: 1245–1258.

54.

Thomas

Hudson

Trauer

, et al. Risk factors for developing prolonged grief during bereavement in family carers of cancer patients in palliative care: a longitudinal study. J Pain Symptom Manage 2014; 47: 531–541.

55.

Kentish-Barnes

Chaize

Seegers

, et al. Complicated grief after death of a relative in the intensive care unit. Eur Respir J 2015; 45: 1341–1352.

56.

Miyajima

Fujisawa

Yoshimura

, et al. Association between quality of end-of-life care and possible complicated grief among bereaved family members. J Palliat Med 2014; 17: 1025–1031.

57.

Mason

Tofthagen

Buck

. Complicated grief: risk factors, protective factors, and interventions. J Soc Work End Life Palliat Care 2020; 16: 151–174.

58.

ONS. Average household income, UK: financial year ending 2022. Newport, UK: ONS, 2023.

59.

Kristensen

Elklit

Karstoft

K-I

. Posttraumatic stress disorder after bereavement: early psychological sequelae of losing a close relative due to terminal cancer. J Loss Trauma 2012; 17: 508–521.

60.

Trevick

Lord

. Post-traumatic stress disorder and complicated grief are common in caregivers of neuro-ICU patients. Neurocriti Care 2017; 26: 436–443.

61.

Djelantik

AMJ

Smid

Kleber

, et al. Do prolonged grief disorder symptoms predict post-traumatic stress disorder symptoms following bereavement? A cross-lagged analysis. Compr Psychiatry 2018; 80: 65–71.

62.

Szuhany

Malgaroli

Miron

, et al. Prolonged grief disorder: course, diagnosis, assessment, and treatment. Focus 2021; 19: 161–172.

63.

Prigerson

. Assessment and associated features of prolonged grief disorder among Chinese bereaved individuals. Compr Psychiatry 2016; 66: 9–16.

64.

Zordan

Bell

Price

, et al. Long-term prevalence and predictors of prolonged grief disorder amongst bereaved cancer caregivers: a cohort study. Palliat Support Care 2019; 17: 507–514.

65.

Breen

Aoun

O’Connor

, et al. Effect of caregiving at end of life on grief, quality of life and general health: a prospective, longitudinal, comparative study. Palliat Med 2020; 34: 145–154.

66.

Tsai

Wen

Kuo

, et al. Symptoms of prolonged grief and major depressive disorders: distinctiveness and temporal relationship in the first 2 years of bereavement for family caregivers of terminally ill cancer patients. Psycho Oncol 2020; 29: 751–758.

67.

Boele

Grant

Sherwood

. Challenges and support for family caregivers of glioma patients. Br J Neurosci Nurs 2017; 13: 8–16.

68.

Tol

Barbui

Van Ommeren

. Management of acute stress, PTSD, and bereavement: WHO recommendations. JAMA 2013; 310: 477–478.

69.

NICE. Post-traumatic stress disorder NG116. Manchester, UK: NICE, 2018.

70.

Byrne

Torrens-Burton

Sivell

, et al. Early palliative interventions for improving outcomes in people with a primary malignant brain tumour and their carers. Cochrane Database Syst Rev 2022; 1(1): CD013440

71.

Piil

Juhler

Jakobsen

, et al. Controlled rehabilitative and supportive care intervention trials in patients with high-grade gliomas and their caregivers: a systematic review. BMJ Support Palliat Care 2016; 6: 27–34.

72.

Heinsch

Cootes

Wells

, et al. Supporting friends and family of adults with a primary brain tumour: a systematic review. Health Soc Care Community 2022; 30: 869–887.

73.

Boele

Rooney

Bulbeck

, et al. Interventions to help support caregivers of people with a brain or spinal cord tumour. Cochrane Database Syst Rev 2019; 7: CD012582.

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