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Nephrol Dial Transplant (2012) 27: 1548–1554

doi: 10.1093/ndt/gfr514
Advance Access publication 6 October 2011

Measuring the quality of end of life management in patients with


advanced kidney disease: results from the pan-Thames renal
audit group

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Stephen P. McAdoo1, Edwina A. Brown1, Alistair M. Chesser2, Ken Farrington3, and Emma
M. Salisbury1 and on behalf of pan-Thames renal audit group
1
Imperial College Kidney and Transplant Institute, Hammersmith Hospital, London, UK, 2Renal Department, Barts and the London
NHS Trust, London, UK and 3Lister Hospital Renal Unit, North Herts NHS Trust, Stevenage, UK
Correspondence and offprint requests to: Stephen P. McAdoo; E-mail: s.mcadoo@imperial.ac.uk

Abstract Introduction
Background. Despite a recent increased awareness of the
need for quality End of Life (EOL) care for patients with Recent years have seen an increasingly aged population
advanced kidney disease, there is no established method for with advanced renal disease who demonstrate significant
measuring or auditing outcomes relating to EOL care in this co-morbidities, a substantial symptom burden and poor
population. survival [1]. Consequently, the need for quality End of
Methods. We designed a one-page proforma, which was Life (EOL) care that attends to the specific needs of this
used to collect data on various aspects of EOL care relating population has been recognized [2]. A decade ago, the
to all deaths of patients on dialysis and patients dying on Renal Physicians Association (RPA) and the American
specialist renal wards, over a predefined 8-week period in
Society of Nephrology published a clinical practice
10 hospitals in London and South–East England.
guideline that emphasized the importance of shared de-
Results. One hundred and thirty-eight deaths were
cision making, informed consent and palliative care for
recorded over the 8-week study period. The majority of
patients with advanced renal disease [3]. More recent
patients (83%) were receiving maintenance haemodialysis
publications, including an update of the RPA guideline
prior to their terminal presentation. About 69% of deaths
in the USA [4] and recommendations issued by the
occurred during an in-patient hospital admission—of these,
Department of Health (DOH) in the UK [5] have reiter-
36% were considered ‘unexpected’ and most quality
ated the importance of providing quality EOL care in this
markers of good EOL management were significantly less
likely to be achieved in these patients, including use of population. Each of these documents describe several
palliative care strategies, good symptom control and overall common features of good quality EOL care, including
quality of death. Thirty-six per cent of patients were from recognition of the dying patient, communication with
various ethnic minorities, and in this group, there was a patients and carers regarding prognosis and desired level
trend towards lower use of palliative care pathways and of care, symptom control and enabling preferred place of
lower rates of withdrawal from dialysis. care. The UK DOH document states that the ‘character-
Conclusions. This study confirms that it is possible to istics of care during the last days of life which have con-
measure many important outcomes relating to quality of sistently been found to be important from the patient’s
EOL care using a proforma completed at the time of death. perspective are adequate pain and symptom management,
Our findings suggest that many aspects of good EOL care avoiding inappropriate prolongation of dying, achieving
are under-achieved in our region. This, in part, is due to a sense of control, relieving burden on loved ones and
a failure to recognize the worsening trajectory of the strengthening relationships with loved ones’, based on
deteriorating patient, resulting in missed opportunities for the previous observations of Singer et al. [6].
EOL care planning and appropriate symptom control. Our Despite these recommendations and increased awareness
observations suggest that there is a need for improved of the need for good EOL care, there is limited data on
education and training in this area, particularly in detection measuring the quality of dying in the advanced renal dis-
of the dying patient, the value of advance care planning and ease population. In 2000, Cohen et al. developed the Dial-
the utility of tools such as the Liverpool Care Pathway. ysis Discontinuation Quality of Dying (DDQOD) tool, a
scoring system to distinguish between good and bad deaths
Keywords: dialysis; end-stage renal disease; palliative care and in a multicentre study involving eight dialysis clinics in
North America found that 38% of patients were judged

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Measuring the quality of EOL management 1549

to have ‘very good deaths’ following withdrawal from Table 1. Demographics, mode of RRT and place of death of the study
dialysis [7]. However, the authors noted several limitations population
of this tool, not least that it was not applicable to patients
Number of patients (%)
who did not withdraw from dialysis prior to death. The
same group have developed the Dialysis Quality of Dying Gendera
Apgar (QODA) for use in all end-stage renal disease Male 78 (57)
(ESRD) patients, although there is no published experience Female 59 (43)
using this tool to date [8], and so, there remains no estab- Age (years)b
lished or validated method for measuring the quality of <30 1 (1)
30–50 16 (12)
EOL care in the ESRD population. 50–70 45 (33)
The aim of the study was to obtain a clinical perspective >70 74 (54)
on the quality of EOL care provided to patients with ad- Ethnicity
vanced kidney disease using a practical and easy to use Caucasian 88 (64)
South-Asian 15 (11)
proforma that was completed at the time of death by a

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Afro-Caribbean 23 (17)
member of the clinical team concerned. Other/unknown 12 (9)
Mode of RRT
Haemodialysis 114 (83)
Materials and methods Peritoneal dialysis 8 (6)
Renal transplant 6 (4)
We designed a one-page proforma (supplementary data) to collect data on Conservative care 10 (7)
various aspects of EOL care, including patient demographics, details of Place of deatha
advance care planning and information relating to actual care delivered Hospital in-patient 94 (69)
during the EOL period. This proforma was used to collect data relating to Home 32 (23)
all deaths of patients on dialysis and patients dying on specialist renal Hospice 8 (6)
wards over a predefined 8-week period. The 12 centres in London and Nursing home 2 (1)
South–East England who participate in the pan-Thames renal audit group Out-patient dialysis unit 1 (1)
were invited to take part. The proforma was completed at the time of death
by senior renal or dialysis nurses or senior medical staff (registrar or a
Data incomplete for one patient.
consultant grade) and returned to a central unit for analysis at the end of b
Data incomplete for two patients.
the 8-week period.
Statistical analysis was conducted using Graphpad Prism (Graphpad
Software, San Diego, CA). Comparison between groups was by Fisher’s
exact test.
renal allograft. The remaining 10 patients had advanced
renal disease and did not receive renal replacement therapy
(RRT) during their illness. This group included those pa-
Results tients who had planned conservative care and those who
‘crash-landed’ in a terminal presentation. As the numbers
are small, we have not analysed outcomes for the planned
Data collection
conservative care patients separately.
Ten of the 12 invited centres returned completed proformas
for deaths occurring over the 8-week period. About 49% of Place of death
the returned questionnaires were completed by senior med-
ical staff (renal registrar or consultant grade), 49% by Sixty-nine per cent of deaths occurred during an in-patient
senior renal or dialysis nurses and 2% were completed by hospital admission. About 23% occurred at home, 6% in a
both medical and nursing staff. To the best of our knowl- hospice and 1% in a nursing home. One death occurred
edge, all deaths during the 8-week study period have been during an out-patient dialysis attendance. The preferred
included. The number of deaths per unit is approximately in place of death was known for 29 patients. Of these patients,
proportion for the prevalent ESRD population for each unit over three quarters (79%) were cared for in their chosen
as recorded by the UK Renal Registry (data not shown). location at the time of death. About 52% of patients for
whom a stated preference was known wanted to die in
hospital, the remainder wanting to die in their home or in
Demographics
a hospice. Thirty-two deaths occurred at home; the majority
In total, 138 deaths (78 male) were recorded from these (91%) of these were ‘sudden and unexpected’.
10 centres. The mean age at death was 68 years (range
27–92). About 64% of patients were Caucasian, 17% Hospital deaths
Afro-Caribbean, 11% south-Asian and the remainder of
other or unknown ethnicity (Table 1). In total, 94 deaths (69%) occurred during an in-patient
hospital admission. Table 2 shows the quality of End of
Life (EOL) management in these patients. The mean length
Mode of renal replacement therapy
of time between admission and death was 19 days,
The vast majority (83%) were receiving maintenance although it should be noted that a significant number of
haemodialysis prior to their terminal presentation (it may deaths occurred within 48 h of admission or after 1 month
subsequently have been withdrawn during the palliative of admission (range 0–99 days) (Figure 1). Dialysis was
care phase). A small number of patients were receiving discontinued in 40% of the 83 patients who were on dial-
peritoneal dialysis (eight patients) and six patients had a ysis at the time of admission to hospital. The average time
1550 S.P. McAdoo et al.
Table 2. Quality of EOL care outcomes for all in-patient hospital deaths pected’ at the time of last admission to hospital. Recogniz-
ing that a patient is at the EOL is a key to enabling a good
Number of patients 94 quality death. We therefore compared standards of manage-
Mean age at death (range)a 68 (40–92) years
Length of admission prior to death (range)b 19 (0–99) days ment in patients whose death was expected or unexpected
‘Do not resuscitate’ order in place 59 (63%) at the time of admission (Table 3). Most quality markers of
Dialysis discontinued prior to death 40 (43%) EOL management were less likely to be achieved in those
EOL Discussion in year prior to death 26 (28%) patients whose death was unexpected. Of the expected
Management changed to palliative care 42 (45%)
Palliative care referral 32 (34%)
deaths, 91% had a Do Not Attempt Resuscitation Order
Liverpool care pathway used 28 (30%) (DNAR) in place, 67% had changed to a palliative care
Patient relatives told patient is dying 60 (64%) approach and 44% used the Liverpool Care Pathway
Good symptom control achieved 49 (52%) (LCP) compared with 23, 18 and 13%, respectively, in
Relatives present at death 53 (56%) the unexpected group. Most strikingly, only 35% patients
‘Good quality death’ as judged by 45 (48%)
person completing proforma or families in the unexpected group had been told that death
was imminent. The percentage of patients having a ‘good

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a
Data incomplete for two patients. quality death’ as judged by the person completing the form
b
Data incomplete for 13 patients. was not high in either group but was lower in the unex-
pected group at 32% compared with 56% in the expected
group.

Ethnicity
Since cultural and religious practices may influence deci-
sions relating to EOL care, we examined the effects of
ethnicity on various aspects of management, shown in
Table 4. As numbers were small for different ethnic
groups, we compared Caucasian to non-Caucasian pa-
tients and included both in-hospital deaths and those that
occurred in the community (home, hospice or nursing
home). A lower percentage of non-Caucasian patients
had their management recorded as being changed from
active to palliative care; associated with this was a lower
Fig. 1. Duration of admission prior to death for those patients who died in
hospital. use of ‘Do Not Resuscitate’ orders, fewer patients having
dialysis discontinued prior to death and lower use of the
LCP. Interestingly, though, symptom control and a ‘good
until death after discontinuation of dialysis was 5.4 days quality death’ were equally achieved in the two groups.
(range 0–20 days). Only 28% of patients who died in
hospital had discussed EOL issues with their medical team Variation between renal centres
in the year prior to death. We went on to examine these
hospital deaths in more detail, as it is in this group of Between 4 and 27 deaths were recorded from each of the 10
patients that there is the greatest potential to improve cur- centres. Numbers are therefore small, so it is not possible to
rent practice given their continuous contact with health care make accurate comparisons between the different centres.
providers. In addition, the majority of non-hospital deaths There was, however, considerable variation. As shown in
were sudden deaths at home with minimal opportunity to Figure 2, for example, care was recorded as changing from
alter management or occurred in hospices where we active to palliative in 18–100% of deaths occurring in
assume EOL care was optimal. individual centres.

Mangement of deaths in hospital. As shown in Table 2,


only 28% of patients or families had recorded discussions Discussion
round the likelihood of death and its management in the
preceding year. Symptoms were recorded as being well This study by the pan-Thames renal audit group is the first
controlled in 52%, though in 22% there appeared to be documented attempt to audit EOL management in patients
no mention in the notes so the question was completed as with advanced kidney disease. The study was limited to
‘unsure’. Care was documented as changing from active to patients receiving RRT and patients dying as in-patients
palliative in 45%, with the palliative care team being in- on specialist renal wards. Patients dying in the community
volved in 34%. The final question on the proforma was ‘In with CKD 5 and not on dialysis, or with a renal transplant,
your opinion, was this a good quality death’ with a footnote were not included.
giving the definition in ‘EOL Care in Advanced Kidney In this study, we have shown that by using a simple one-
Disease: a framework for implementation’ [5]. Only 48% page document completed at the time of death, many as-
of deaths were recorded as good quality. pects relating to the quality of EOL care can be measured
and quantified. While some of the information gathered
Unexpected and expected deaths in hospital. Thirty-six remains subjective to a degree (such as judgements relating
per cent of all in-patient deaths were considered ‘unex- to inappropriate prolongation of or overall ‘quality’ of
Measuring the quality of EOL management 1551
Table 3. Comparison of quality of EOL outcomes in expected and unexpected in-patient deaths

Unexpected death Expected death

Number of patientsa 34 patients 57 patients


Mean age at death, years (range) 62 (42–84) years 72 (40–92) years
Length of admission prior to death (range)b 13 (0–76) days 23 (0–99) days
‘Do not resuscitate’ order in place* 24% 91%
Dialysis discontinued prior to death* 18% 58%
Management changed to palliative care* 18% 67%
Palliative care referral* 12% 46%
LCP used* 13% 44%
Patient/relatives told patient is dying* 35% 89%
Good symptom control achieved 47% 58%
Relatives present at death 50% 63%
‘Good quality death’ as judged by person 32% 56%

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completing proforma*
a
Three patients classified as ‘unsure’ not included in subsequent analysis.
b
Data incomplete for 10 patients.
*P < 0.05.

Table 4. Comparison of quality of EOL outcomes in Caucasians and non-Caucasians

Caucasian Non-Caucasian

Number of patients 88 (64%) 50 (36%)


Mean age at death (range)a 70 (27–89) years. 63 (45–92) years.
‘Do not resuscitate’ order in place 55% 46%
Dialysis discontinued prior to death 52% 36%
Management changed to palliative care 45% 32%
LCP used 31% 18%
Patient/Relatives told patient is dying* 33% 50%
Good symptom control achieved 53% 54%
Relatives present at death* 48% 68%
‘Good quality death’ as judged by person 51% 52%
completing proforma
a
Data incomplete for two patients.
*P < 0.05.

death) much of it can be used to objectively describe the The failure to have EOL discussions is not in keeping
quality of EOL care and to establish if its provision is in with the findings of Davison [11], who found that in a
keeping with the wishes of patients and their families, and group of patients with advanced kidney disease, the most
if the recommendations of recently published national valued elements of EOL care were being informed about
documents are being implemented. prognosis, being informed about treatment options (includ-
Renal palliative care literature and guidelines suggest ing withdrawal from dialysis) and being able to prepare and
that the principal elements of good EOL care for the patient plan for death. In addition, a recent study in an oncology
with advanced kidney disease include advance care plan- population found that, despite physicians’ concerns about
ning to establish agreed level of care and preferred place of the possible adverse psychological impact of EOL discus-
care, appropriate change of emphasis from active to pallia- sions, patients who did not recall having these discussions
tive care including potential withdrawal of dialysis, con- had more aggressive medical care with a poorer quality of
tinuing discussions with patient and family and symptom life in the last days of life, with no evidence to suggest that
control at EOL [9]. Our results suggest that many of these discussions resulted in emotional distress or psychiatric
elements are under-achieved, particularly in patients dying disorders [12]. Similarly, a recent randomized control trial
in hospital. Of these patients, for example, only 28% had found that facilitated advance care planning in an elderly
discussed their EOL care with medical or nursing staff in population was associated with improved EOL care [13]. It
the year before death, and only 64% patients/families had a is notable that the favoured time for these discussions,
recorded discussion about dying during their final admis- according to Davison’s study, was at a time of serious ill-
sion. At the time of death, only 52% were recorded as ness or ‘when the need arises’, so it is striking that only
having good symptom control and 30% were on the 64% of our hospitalized population were told death was
LCP, despite the recommendation as a useful tool at the imminent during their final admission to hospital, and only
EOL and the availability of adapted versions that are suit- 28% were documented to have had EOL discussions in the
able for use in the advanced kidney disease population [10]. year prior to this admission. About 43% of these patients
Overall, only 48% of deaths were deemed to be of good had dialysis discontinued before death and 45% had
quality by the person completing the form. changed to a palliative care strategy, despite documented
1552 S.P. McAdoo et al.

the LCP, suggesting that their terminal care and symptom


management may not be optimal and a need for increased
awareness of the adapted LCP for patients with renal disease.
Over a third of in-patient deaths were considered as
unexpected at the time of their final admission to hospital
by their health care team, despite the fact that many were
elderly, were on dialysis, had significant co-morbidities and
died, on average, only 13 days later. This suggests that
there were often unrealistic expectations regarding out-
comes of treatment and failure to recognize the deteriorat-
ing trajectory of the patient. Unexpected death was
associated with more failed attempts at resuscitation, lower
use of palliative care strategies, poorer symptom control
Fig. 2. Proportion of patients at each individual unit who were changed and overall poorer quality of death. Improving recognition

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from active to palliative management during their terminal presentation. of the EOL phase should result in improved quality of care.
The first RPA guidelines were published over a decade ago
EOL care discussion in only 28%. Such discussions are and since then many methods of identifying those patients
often poorly documented, and this may account in part who are approaching the EOL have been described,
for these somewhat conflicting observations. However, including ‘the surprise question’ [17], the Gold Service
we would expect that where any preferences were ex- Framework prognostic indicators [18] and ‘Cause for
pressed or decisions made, these should have been Concern’ registers. Despite this, however, our observations
recorded. Our findings underscore the importance of clear suggest that there remains an unmet need for improved
documentation in case records to ensure patient’s wishes education in the geriatric and palliative aspects of care in
are recorded and shared with all involved caregivers, allow- nephrology. The explicit inclusion of these strategies as
ing the principles of shared decision making and informed core elements of training curricula and as local and national
consent to be upheld. In addition, our study did not identify audit criteria may improve the quality of EOL care for those
those patients who were not able, or chose not, to engage in with advanced kidney disease. Although the recent devel-
EOL discussions, which may account in part for these opment of a national strategy for EOL care in the UK is
findings, though highlighting the importance of advance encouraging, it is notable and disappointing that the recent
planning for EOL care before patients become too unwell National Institute for Health and Clinical Excellence
or incapacitated by illness to express their informed wishes. (NICE) Quality Standards for patients with chronic kidney
Twenty-three per cent of deaths in our study occurred at disease do not include a standard for EOL care [19].
home, which is in slightly above the national average (19%) A third of the patients were from various ethnic minor-
for patients with terminal illnesses in England [14]. ities; this is not surprising given the large number of dif-
However, the vast majority of home deaths in our study were ferent ethnic communities in London and the higher
‘sudden’ or unexpected and are thus not reflective of a prevalence of end-stage kidney disease in non-Caucasians.
‘terminal’ population. Studies suggest that the majority of The lack of access to, and uptake of, palliative care services
people with terminal illnesses would prefer to die at home by some ethnic minority groups was established >15 years
[15], and Davison found that only one quarter of patients ago [20] and more recent evidence suggests that this disparity
with advanced kidney disease wanted to die in hospital [11]. may be maintained in some groups across the UK [21, 22].
As such, our figures may well reflect a failure to meet our We therefore examined the effects of ethnicity on the
patients’ preferences. Of concern, however, is that we do not quality of EOL care in our population. While their families
know our patients’ preferences—the favoured place of death were more likely to informed of their prognosis and to be
was not known for almost 80% of patients in this study, present at the time of death, we observed a trend that pa-
again reflecting a failure to discuss patients’ EOL care and tients from ethnic minorities were less likely to withdraw
provide the opportunity for advance planning. from dialysis and less likely to move to a palliative care
Patients with renal disease have a significant complex pathway (including use of the LCP) prior to death. This
symptom burden requiring careful management and argu- may reflect language and actual or perceived cultural bar-
ably would benefit from the involvement of specialist riers to EOL discussions or changing from active to pallia-
palliative care services. Findings of a recent survey suggest tive care. The challenge of providing a comprehensive,
that the majority of palliative care services in the UK now culturally appropriate palliative care service and the need
accept ESRD patients but that limited numbers are referred for ongoing research to establish the EOL needs of different
[16], in keeping with our observation that only 34% patients populations, is well recognized.
were referred to specialist palliative care. It may be sug- Our study has several limitations. The use of a
gested that renal teams are increasingly able to provide pal- questionnaire-based method for data collection has obvious
liative care for their patients and that this may account for a constraints; it is dependent on the required information being
lower than expected referral rate to specialist services. In- recorded in the notes and on a subjective judgement by the
deed, continuing care delivered by a familiar team with person completing the form. We noted a high degree of
whom relationships have been developed over long periods variation between individual renal units in some domains
of time may be preferable to patients. However, our data of the questionnaire, such as the proportion of patients
shows that even fewer patients (30%) were managed using changed to a palliative care aim shown in Figure 2. Numbers
Measuring the quality of EOL management 1553

were too small to allow comparison between units. Areas of these strategies are to succeed [24]. It is hoped that this
particularly outstanding or poor care may not have been and future work, including the completion of the audit
detected, therefore, as a result of our grouped analysis. ‘cycle’ once the UK DOH national strategy has had an
The greatest challenge presented by this study is defin- opportunity to be embedded in practice, will raise awareness
ing what constitutes ‘a good quality’ death. The proforma of the need for improvement, while providing a means to
included a footnote giving the definition used in the UK further define and audit the standards that we should aim to
DOH document. However, this is arguably a highly sub- achieve.
jective definition and issues relating to inappropriate pro-
longation and overall quality of death are clearly difficult
to interrogate in detail using a closed question proforma- Supplementary data
based method (though it is notable that only a minority of
respondents chose ‘unsure’ for any given domain on the Supplementary data are available online at http://
questionnaire). In future cycles of this audit, it would ndt.oxfordjournals.org.
be desirable to clarify some of the terminology used on

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the questionnaire and to train the involved staff in the Acknowledgements. We thank all those who helped coordinate the data
interpretation and completion of the proforma. collection and complete the proformas: Michele Cafferkey, Basildon Hos-
That the proformas were completed by nursing and pital; Sue Cox, Guys Hospital; Wendy Brown, Hammersmith Hospital;
Bernhard Klebe, Kent and Canterbury Hospital; Miriam Ball, Lister Hos-
medical staff directly involved in patient care may have pital; Andrew Davenport, Royal Free Hospital; Mike Almond, Alistair
affected the objectivity of our results, and this is likely to Chesser, Royal London Hospital, Southend Hospital; Angela Reed, St
be an inherent problem of many studies in this area. The George’s Hospital; David Makanjuola, St Helier Hospital.
VOICES (Views Of Informal Carers: Evaluation of Serv-
ices) questionnaire (part of the PROMOTE project; The Conflict of interest statement. None declared.
Project to impROve Management Of TErminal illness
[23]) was identified as a useful tool to be completed retro- (See related article by Arulkumaran et al. End-of-life care in patients with
spectively by bereaved relatives or carers to evaluate the end-stage renal disease. Nephrol Dial Transplant 2012; 27: 879–881.)
quality of care provided to patients at the EOL, and the use
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