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Palliative Medicine

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The association between in-patient death, utilization of hospital resources and availability of palliative
home care for cancer patients
Alberto Alonso-Babarro, Jenaro Astray-Mochales, Felicitas Domnguez-Berjn, Ricard Gnova-Maleras, Eduardo Bruera,
Antonio Daz-Mayordomo and Carlos Centeno Cortes
Palliat Med 2013 27: 68 originally published online 4 April 2012
DOI: 10.1177/0269216312442973

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42973 PMJ27110.1177/0269216312442973Alonso-Babarro et al.Palliative Medicine

PALLIATIVE
Original Article MEDICINE
Palliative Medicine

The association between in-patient


27(1) 6875
The Author(s) 2012
Reprints and permission:
death, utilization of hospital resources sagepub.co.uk/journalsPermissions.nav
DOI: 10.1177/0269216312442973

and availability of palliative home care pmj.sagepub.com

for cancer patients

Alberto Alonso-Babarro Palliative Care Unit, Hospital Universitario La Paz, Spain

Jenaro Astray-Mochales Direccin General de Atencin Primaria, Consejera de Sanidad, Comunidad de Madrid, Spain

Felicitas Domnguez-Berjn Direccin General de Atencin Primaria, Consejera de Sanidad, Comunidad de Madrid, Spain

Ricard Gnova-Maleras Direccin General de Atencin Primaria, Consejera de Sanidad, Comunidad de Madrid, Spain

Eduardo Bruera Department of Palliative Care and Rehabilitation Medicine, The University of Texas, MD Anderson Cancer Center, USA

Antonio Daz-Mayordomo Centro de Salud Tres Cantos, Spain

Carlos Centeno Cortes Equipo de Medicina Paliativa, Clnica Universitaria de Navarra, Spain

Abstract
Background: The impact of palliative home care programs on in-patient admissions and deaths has not been appropriately established.
Aim: The main objectives of this study have been to evaluate the frequency of in-patient hospital deaths and the use of hospital
resources among cancer patients in two areas of the Madrid Region, as well as to assess differences between one area with and one
without a palliative home care team (PHCT) in those variables.
Design and setting: We conducted a population-based study comparing two adjacent metropolitan areas of approximately 200,000
inhabitants each in the Madrid Region, Spain, measuring in-patient deaths, emergency room admissions and in-patient days among
cancer patients who died in 2005. Only one of the two areas had a fully established PHCT.
Results: 524/549 cancer patients (95%) had an identified place of death: 74% died in hospital, 17% at home, 6% in an in-patient hospice
and 3% in a nursing home. The frequency of hospital deaths was significantly lower among patients of the PHCT area (61% versus
77%, p < 0.001), as well as the number of patients using emergency and in-patient services (68% versus 79%, p = 0.004, and 66 versus
76%, p = 0.012, respectively). After adjusting for other factors, the risk of hospital death was lower among patients older than 80 (OR,
95% CI, 0.3, 0.10.5), higher among patients with hematological malignancies (OR 6.1, 2.018.9) and lower among patients of the PHCT
area (OR 0.4, 0.20.6).
Conclusions: Our findings suggest that a PHCT is associated with reduced in-patient deaths and overall hospitalization over the last
two months of life.

Keywords
Place of death, cause of death, death certificate, palliative care, cancer, hospital mortality, home care services, hospital based, age
factors, socioeconomic factors

Introduction frequent in-patient admissions.9,10 In the USA, the structure


and availability of healthcare resources appear to influence
Most patients with advanced cancer prefer to receive care place of death more than the actual preference of patients
and die at home.1,2 However, most patients die in hospital.28 and families.1113 Some studies have suggested that home
During the last months of life, cancer patients undergo care teams decrease the number and duration of in-patient

Corresponding author:
Dr Alberto Alonso-Babarro, Unidad de Cuidados Paliativos, Hospital La Paz, Po Castellana 261, 28046 Madrid, Spain.
Email: albertoalonsob@gmail.com

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Alonso-Babarro et al. 69

admissions and increase the rate of home deaths.1422 now on will referred to as the PHCT Area. Area 2 [named
However, the number of studies is small, there is quite a Alcala de Henares] had no access to a PHCT in 2005 and
variable level of physician participation and the role of from now on will be referred to as the Non-PHCT Area.
these home-based programs in reducing the rate of hospital Both health areas had full access to major university hospitals,
deaths among cancer patients has not been completely oncology services, family physicians and in-patient
established.23 Health regions around the world have hospice beds.
attempted to establish palliative care programs as a way of Average income per capita in the Non-PHCT Area was
improving the quality of life of terminally ill patients and similar to the average Spanish income, while in the PHCT
their families and also as a way of reducing utilization of Area, one of the sub-areas [San-Sebastian de Los Reyes]
expensive acute care hospital resources.24,25 had approximately 20% above-mean income, and the
The percentage of patients dying in hospital as com- other sub-area [Alcobendas] approximately 50% above
pared to those dying at home, and the possibility of spend- the Spanish mean income.30 The PHCT Area also had a
ing most of the last weeks of life at home, have been utilized higher availability of acute hospital beds (2.2 versus 1.6
as quality indicators of palliative care programs.26 Although beds per 1000 people).
there are several limitations, these measures can be used to
evaluate programs over time, as well as to compare the
Study design
impact of different programs on care at the end of life.3,6,7,14
22,27,28 The World Health Organization (WHO) and a num- We reviewed cancer deaths for 2005 for all adult cancer
ber of other international organizations have focused on the patients over 18, in both health regions. The Madrid
importance of research in factors associated with place of Regional Statistics Institute (IECM) provided the individ-
death in different regions of the world.29 ual data of deceased patients.
In this population-based study, we sought to investigate This study was approved by the Institutional Review
the frequency of in-patient hospital death and the use of Board of the Primary Care Program of each of the two
hospital resources (measured as emergency room admis- health areas. Appropriate authorization was obtained from
sions, in-patient admissions and in-patient days) in two the Madrid Regional Government and the Data Protection
metropolitan areas of the Madrid Region. We hypothesized Agency.31
that a palliative home care team (PHCT) established in one In Spain the death certificate has two components: one
of these areas could influence those variables. of them is called the Medical Death Certificate (MDC),
which includes the address where the death took place.
The other component is the Statistic Death Bulletin (SDB)
Methods which is used for statistical purposes and includes the
patients main diagnosis and other demographic charac-
Study location teristics. Since 2009, a new document has been imple-
The Madrid Region has a population of approximately 6 mented, containing both MDC and SDB information in a
million, essentially of an urban nature (94%). All residents single form and including a new place-of-death checklist.
of the Region have access to universal healthcare provided In order to double-check the appropriate place of death,
by the National Health System. we cross-linked the information from the MDC regarding
In 2006 the Madrid Region activated an integrated pal- address with the Tanatos Registry kept by funeral directors.
liative care program aimed at providing universal access to This registry determines the exact address where a body
all levels of palliative care services for the community. has been collected for funerary purposes.
Until that year, resource distribution was highly irregular In-patient care data were obtained from the register of
among the different regional healthcare areas. Six of the the public and private hospitals of the Madrid Region, and
eleven health areas established a PHCT in 1998. Patients emergency room visit data were obtained from the register
living in an area without a PHCT could not use the PHCT of the major public hospitals available in the health regions.
from the other areas. Each team provided care to 300,000 All the institutions kept electronic activity records. We only
700,000 inhabitants. The team was composed of two physi- considered the last two months before death [62 days] for
cians, two nurses, an assistant nurse and an administrative the purpose of this study. We used the PHCT Register to
clerk. The PHCTs conducted regular follow-up of patients check the patients who had been followed up by this Team.
referred by acute care hospitals, medical oncologists or
family physicians when these patients were perceived by
Variables
the referring physician as having a progressive incurable
disease and high symptom distress. We classified the cause of death according to International
We compared two adjacent areas of approximately Classification of Diseases (ICD)-10 and, for the purpose of
200,000 inhabitants each. Area 1 [named Alcobendas-San- this study, we used all the codes corresponding to neoplas-
Sebastian de Los Reyes] had access to a PHCT and from tic diseases. These include, according to anatomic location,

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70 Palliative Medicine 27(1)

digestive tract codes, C00C26, C48, C451; respiratory of the two different areas. Hospital death frequency was
codes, C30C34, C37C39, C45.0, C45.2; breast code, significantly lower among patients in the PHCT Area (61%
C50; genitourinary codes, C51C58, C60C68; hemato- versus 77%, p < 0.001). The PHCT Area patients used
logical codes, C81C85, C88C96, D46; and other codes, emergency services and in-patient services less frequently
C40, C41, C43, C44, C49, C69C80, C97, C457C479, than those in the Non-PHCT Area (68% versus 79%, p =
D00D45, D47, D48. 0.004, and 66 versus 76%, p = 0.012, respectively).
Other variables include demographic characteristics, Table 2 summarizes the probability of hospital death
such as age, gender, marital status and place of residence. and differences in both bi-variant and multi-variant anal-
For the purpose of socioeconomic level we used a depri- yses. After adjusting for other factors, patients in the
vation index based on residence census information. This PHCT Area and patients aged over 80 had a significantly
index has been elaborated for small areas (census tracts lower risk of hospital death, whereas the risk among
with a median of 1000 inhabitants) of the Madrid Region patients with hematological malignancies was signifi-
based on several census (2001) indicators,32 and the areas cantly higher. In the bi-variant analysis, the risk of hospi-
have been categorized into quintiles in which the fifth is the tal deaths was significantly higher among patients with
most unfavorable one. lower socioeconomic levels. There was no difference by
With regard to healthcare utilization, we determined in- gender or marital status.
patient hospital care within the last two months before The probability of a hospital death increased in direct
death, access to a PHCT, number of times the patient was relationship with the number of visits to the emergency
seen by an emergency room and total number of days the center and/or the in-patient hospital and with the number of
patient remained admitted during the study period. Visiting in-patient days. The mean of in-patient days during the last
the emergency room did not mean being admitted to the two months of life among patients who died at home, hav-
hospital, so we collect data about both variables. ing been admitted at least once, was 7, versus 17 among
patients who died in hospital [p < 0.001].
Table 3 summarizes the differences according to place
Data analysis
of death and hospital utilization between patients followed
We analyzed the probability of dying in hospital in accord- up by a PHCT and those who did not receive this kind of
ance with different sociodemographic and clinical varia- assistance at home (in the PHCT Area and in the Non-
bles and in accordance with the assistance of a PHCT PHCT Area). PHCT patients had a higher percentage of
using bi-variate and multi-variate analysis by logistic home deaths compared with the rest of the patients (67.6%
regression. We calculated the odds ratio and 95% confi- versus 12.5%, OR after adjusting for other factors [95% CI]
dence interval (CI) using the statistical package for the 23.4, 9.160.0).
social sciences (SPSS V15).

Discussion
Results To our knowledge this is one of the first population-based
There were a total of 549 adult cancer deaths in the two studies addressing the association between hospital mortal-
areas during 2005. The age-adjusted population mortality ity and presence of a PHCT in two areas within the same
rate according to the Standard European Population was healthcare system, and one of the first population-based
2.23 cancer deaths per 1000 inhabitants. The rate was the studies to analyze place of death in Spain. A study has been
same in the two areas. published recently about place of death in Andalusia
In the vast majority of cases the place of death was (Spain) in 2009 using the Death Certificate, but the authors
obtained from the MDC and/or the Tanatos Registry. There could only find less than 50% of the patients places of
were 10 cases of disagreement between Tanatos and the death.33
MDC and, in such cases, the Tanatos-registered place of Our study found that the frequency of in-patient hospital
death was used as the appropriate location. In 21 cases deaths and use of hospital resources during the last two
where this information was not available, the information months of life was significantly lower in the PHCT Area.
was ultimately available from hospital medical records. The risk of a hospital death was significantly lower when
In 25 [4.6%] cases the exact place of death could not be patients had access to a PHCT, after adjusting for other fac-
determined. tors [OR 0.4, 95% 0.20.6]. The two healthcare areas
Overall, 524 patients were studied for place of death. A belong to the urban part of the Madrid Region and they are
total of 387 (74%) patients died in hospital, 90 (17%) died part of the same healthcare system. Patients have access to
at home, 29 (6%) died in an in-patient hospice and 18 (3%) the same level of family physician coverage, medical
died in a nursing home. oncology specialists and tertiary hospital in-patient admis-
Table 1 summarizes the differences by place of death sions. Clinical and demographic characteristics of patients
and other sociodemographic and clinical variables in each in both areas were quite similar. In spite of everything, the

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Alonso-Babarro et al. 71

Table 1. Patient clinical and demographic characteristics in the palliative home care team (PHCT) and Non-PHCT Areas.

Non-PHCT Area PHCT Area p


N % N %
TOTAL 323 226
Gender
Female 113 35.0 77 34.1 0.825
Male 210 65.0 149 65.9
Age at death (years)
<65 114 35.3 94 41.6 0.217
6579 126 39.0 73 32.3
80+ 83 25.7 59 26.1
Marital status
Single 29 9.0 16 7.1 0.528
Married 215 66.6 148 65.5
Widowed 65 20.1 55 24.3
Separated or divorced 14 4.3 7 3.1
Socioeconomic status
Quintile 1 (highest) 22 6.8 46 20.4 <0.001
Quintile 2 47 14.6 26 11.6
Quintile 3 54 16.7 73 32.4
Quintile 4 60 18.6 69 30.7
Quintile 5 (lowest) 140 43.3 11 4.9
Cancer type
Gastrointestinal 93 28.8 69 30.5 0.261
Lung 79 24.5 61 27.0
Breast 17 5.3 14 6.2
Genitourinary 50 15.5 19 8.4
Hematological 32 9.9 21 9.3
Others 52 16.1 42 18.6
Place of death
Home 42 13.0 47 20.8 <0.001
Hospital 249 77.1 138 61.1
In-patient hospice 3 0.9 26 11.5
Nursing home 14 4.3 5 2.2
Unknown 15 4.6 10 4.4
Visited the emergency rooma
No 68 21.1 72 31.9 0.004
Yes 255 78.9 154 68.1
Mean number of visits 1.46 1.09 <0.001
Admitted to the hospitala
No 77 23.8 76 33.6 0.012
Yes 246 76.2 150 66.4
Mean number of admissions 1.00 0.87 0.043
Emergency room visits and admissions
No 26 8.0 40 17.7 0.001
Yes 297 92.0 186 82.3
Mean number of visits/admissionsa 2.08 1.72 <0.001
aLast 62 days before death

differences we found between the PHCT and the Non- differences seem to suggest that the PHCT allowed patients
PHCT Areas may not necessarily have been due to the pres- to remain out of the in-patient hospital facilities and to die
ence of the PHCT, but to other regional differences we did more commonly in a non-hospital setting. Our findings
not measure. However, when comparing both regions for regarding patients followed up by the PHCT are similar to
only those patients who did not make use of the PHCT, those reported recently by our group in an observational
there were no large differences. Therefore, the observed cohort study.34 The PHCT seems to be the strongest factor

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72 Palliative Medicine 27(1)

Table 2. Risk of in-patient hospital death according to clinical and demographic characteristics.

N % In-patient Odds ratio 95% CI Adjusted odds 95% CI


hospital deaths ratioa
TOTAL 549 70.5
Gender
Female 190 67.9 1 1
Male 359 71.9 1.2 0.81.8 1.2 0.72.0
Age at death (years)
<65 208 77.9 1 1
6579 199 75.9 0.9 0.61.5 0.8 0.51.3
80+ 142 52.1 0.3 0.20.5 0.3 0.10.5
Marital status
Single 45 77.8 1 1
Married 363 74.7 0.9 0.41.9 0.8 0.31.8
Widowed 120 55.0 0.4 0.20.9 0.7 0.31.8
Separated or divorced 21 71.4 1.0 0.33.6 0.8 0.23.1
Socioeconomic status
Quintile 1 (highest) 68 58.8 1 1
Quintile 2 73 60.3 1.1 0.52.1 0.9 0.41.9
Quintile 3 127 71.7 1.8 0.93.4 1.8 0.93.7
Quintile 4 129 72.9 1.8 1.03.5 1.8 0.93.7
Quintile 5 (lowest) 151 78.1 2.7 1.45.3 1.8 0.83.9
Cancer type
Gastrointestinal 162 66.7 1 1
Lung 140 66.4 1.0 0.61.7 0.7 0.41.3
Breast 31 74.2 1.2 0.52.9 1.1 0.43.0
Genitourinary 69 69.6 1.1 0.62.0 0.9 0.51.9
Hematological 53 90.6 5.0 1.714.7 6.1 2.018.9
Others 94 71.3 1.3 0.72.3 1.2 0.62.2
Palliative home care
Non-PHCT Area 323 77.1 1 1
PHCT Area 226 61.1 0.4 0.30.6 0.4 0.20.6
aAdjusted Odds Ratio (OR) and 95% confidence interval (CI) from a multiple logistic regression model with all variables listed in the table.

PHCT: palliative home care team

to explain differences between the PHCT Area and the They enrolled 434 patients who had incurable malignant
Non-PHCT Area regarding place of death and hospital uti- disease and an expected survival of 29 months. More
lization by cancer patients who died in the study areas. In patients receiving palliative care were able to die at home,
Canada, similar findings have been reported when compar- although time spent at home was not significantly
ing hospital deaths and total in-patient days of the last increased and overall hospital utilization was similar in
admission before and after the inception of a regional pal- both groups. Brumley et al.21 randomized 298 terminally
liative care program.35 A study in Belgium strongly relates ill patients to usual care versus in-home palliative care
place of death with involvement of palliative care ser- plus usual care delivered by an interdisciplinary team.
vices.22 They found that patients randomized to home palliative
A number of studies have attempted to establish the care were more likely to die at home and less likely to visit
relationship between home palliative care programs and the emergency department or be admitted to the hospital
in-patient deaths. Grande et al.15 randomized 229 pallia- than those receiving usual care. The authors suggested
tive care patients to hospital-at-home versus standard that this resulted in a significant decrease in care cost.
care. Patients admitted to hospital-at-home were more Our findings are consistent with those of the rand-
likely to die at home than controls. However, the findings omized controlled trials. One of the limitations of clinical
were limited, since a number of patients allocated to one trials is the relatively artificial environment created by
of the treatment groups did not receive such treatment. eligibility criteria and settings where these studies are con-
Jordhy et al.20 conducted a cluster randomized control trial ducted. It is encouraging that our population-based study
of a palliative care intervention versus conventional care. supports the fact that a relatively simple physician- and

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Alonso-Babarro et al. 73

Table 3. Differences according to place of death and hospital utilization between patients followed up by a palliative home care
team (PHCT) and those who did not receive this kind of assistance at home (in the PHCT Area and in Non-PHCT Area).

Patients in the Patients in the PHCT Patients followed up p value


Non-PHCT Area Area who did not by the PHCT
receive assistance from
the PHCT

N % N % N %
TOTAL 323 100.0 189 100.0 37 100.0
Place of death
Home 42 13.0 22 11.6c 25 67.6c <0.001
Hospital 249 77.1 133 70.4c 5 13.5c
In-patient hospice 3 0.9b 21 11.1b 5 13.6
Nursing home 14 4.3 5 2.6 - -
Unknown 16 4.6 8 4.2 2 5.4
Number of emergency room visitsa
0 68 21.1 56 29.6 16 43.2 0.001
1 105 32.5 70 37.0 13 35.1
2 82 25.4 43 22.8 7 18.9
3+ 68 21.1b 20 10.6b 1 2.7
Number of admissionsa
0 77 23.8 54 28.6c 22 59.5c <0.001
1 180 55.7 98 51.9 12 32.4
2+ 66 20.4 37 19.6 3 8.1
Number of emergency room visits and admissionsa
0 26 8.0 25 13.2c 15 40.5c <0.001
1 71 22.0 47 24.9 6 16.2
2 77 23.8 53 28.0 10 27.0
3+ 149 46.1b 64 33.9b 6 16.2
aLast 62 days before death.
bStatistically significant (p < 0.05) between patients in the Non-PHCT Area and patients in the PHCT Area who did not receive assistance from the
PHCT.
cStatistically significant (p < 0.05) between patients followed up by the PHCT and patients in the PHCT Area who did not receive assistance from the

PHCT.

nurse-based palliative home care intervention is capable of Our study found that patients with lower socioeconomic
significantly reducing the number of in-patient deaths. status had a higher risk of an in-patient death. A number of
Since the vast majority of the cost of end-of-life care is studies have made similar findings.34,38,39 A Swedish study
related to in-patient care, our findings could be encourag- observed no significant association between income and in-
ing as a potential for substantial cost savings. However, patient deaths.40 These findings might reflect the outstand-
cost savings are predominantly linked with the number of ing level of Swedish social services, including intensive
days of in-patient care during the last months of life, rather home support and paid leave of absence for relatives. Some
than the actual location of death. More research is required authors suggest that level of social support is one of the
to better determine if PHCTs are capable of reducing not most important factors that influence place of death.4143
only the number of in-patient deaths, but also the overall These findings could be important for the planning of pal-
duration of in-patient days during the last months of life. liative home care programs. Programs in areas where there
Our findings regarding in-patient admissions and total is higher socioeconomic level and social support should be
number of in-patient days during the last two months of life expected to be able to achieve higher rates of home death.
are consistent with those of studies conducted in Canada Programs should pay specific attention to patients with
and Belgium.9,10 These findings emphasize the very large lower socioeconomic status in order to develop appropriate
cost of caring for advanced cancer patients in the last policies addressing their needs.
months of life. Unfortunately, this high cost of acute care Regarding the remaining demographic variables (includ-
institution admissions does not seem to correlate with ing age, gender and marital status), only age had significant
better symptom control and overall family distress, particularly association with place of death. People over 80 had the
for those patients who die in hospital.36,37 highest proportion of home deaths. Our findings are similar

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74 Palliative Medicine 27(1)

to those found in Italy, but opposite to other European Funding


countries. This could be a characteristic common to Dr Eduardo Bruera is supported in part by the National Institutes
Mediterranean countries and exemplifies how cultural of Health (Grant numbers RO1NR010162-01A, RO1CA122229-
differences determine patterns in place of death.13,38 01 and RO1CA124481-01).
Our findings regarding a significantly higher risk of in-
patient death among patients with hematological malig-
Conflict of interest statement
nancy are consistent with those of our group and others
showing a higher in-patient mortality rate, higher num- The authors declare that there is no conflict of interest.
bers of intensive care unit (ICU) deaths and later referral
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