Iea Van Oostrum
email: ivanoostrum@ggd.nl

PhD S Goosen

D G Uitenbroek

Prof K Stronks

Mortality and causes of death among asylum seekers in the Netherlands, 2002-2005

Keywords: Asylum seekers, Refugees, Migrants, Mortality, Preventive Health Services

Background: The world's growing population of asylum seekers faces different health risks than the populations of their host countries due to pre-and post-migration risk factors. We currently lack insight into their health status.

Methods:

We designed a unique notification system to monitor mortality in Dutch asylum seeker centres (2002)(2003)(2004)(2005).

Results: Standardized for age and sex, the overall mortality rate among asylum seekers shows no difference with the Dutch population. However, rates differ between subpopulations by sex, age and region of origin and by cause of death. Mortality among asylum seekers was higher than among the Dutch reference population at younger ages and lower at ages above 40. The most frequent causes of death groups among asylum seekers are cancer, cardiovascular diseases, and external causes. We found increased mortality due to infectious diseases (males SMR=5.44; 95% CI 3.22-8.59, females SMR=7.53; 95% CI 4.22-12.43), external causes (males SMR=1.95; 95% CI; 0.52-2.46, females SMR=1.60; 95% CI 0.87-2.68), and congenital anomalies in females (SMR 2.42; 95% CI 1.16-4.45). Considerable differences were found between regions of origin. Maternal mortality was increased (rate ratio 10.08; 95% CI 8.02-12.83) as a result of deaths among African women.

Conclusion:

Subgroups of asylum seekers by age, sex and region of origin, are at increased risk for certain causes of death in comparison to the host population. Policies and services for asylum seekers should address both causes for which asylum seekers are at increased risk and causes with large absolute mortality, taking into account differences between subgroups.

What this paper adds

What is already known on this subject?

• Data about differences in overall and cause-specific mortality between asylum seekers and the general population in their western host countries are not available internationally.

What does this study add?

• This study provides insight in mortality and causes of death among asylum seekers in the Netherlands.

• Mortality patterns are not homogeneous -there are great differences between subgroups by sex, age, region of origin; overall and for specific causes of death.

• Main causes of death are cancer, cardiovascular diseases, and external causes. Excess mortality compared with the host country population was large for infectious diseases, external causes, and mortality associated with pregnancy and childbirth.

• Health policies and services for asylum seekers should address both causes for which asylum seekers are at increased risk and causes with large absolute mortality, taking into account differences between subgroups.

INTRODUCTION

Of the estimated 11.4 million refugees worldwide in 2007,[1] 760,000 asylum seekers lived in Western countries. Presumably, pre-and post-migration factors are risks to asylum seekers' health, [START_REF] Norredam | Access to health care for asylum seekers in the European Union -a comparative study of country policies[END_REF] as are genetic factors, [START_REF] Bischoff | The self-reported health of immigrant groups in Switzerland[END_REF][START_REF] Wiking | Ethnicity, acculturation, and self reported health.A population-based study among immigrants from Poland, Turkey, and Iran in Sweden[END_REF] and stress factors before and during their flight from war-struck countries. Some authors mention limited access to healthcare as a negative factor. [START_REF] Norredam | Migrants' access to health care[END_REF][START_REF] Burnett | Asylum seekers and refugees in Britain. Health needs of asylum seekers and refugees[END_REF][START_REF] Adams | Health care challenges from the developing world; Post-immigration refugee medicine[END_REF] Asylum seekers are thought to be subject to specific health problems, [START_REF] Burnett | Asylum seekers and refugees in Britain. Health needs of asylum seekers and refugees[END_REF][START_REF] Adams | Health care challenges from the developing world; Post-immigration refugee medicine[END_REF] of which infectious diseases and mental health problems receive the most attention.

Little evidence about the health of asylum seekers in Europe is available, however, there is not much systematic research; it is done on too small a scale or is limited to qualitative data. In quantitative studies, such as those based on national mortality statistics, it is impossible to distinguish asylum seekers from other migrants, [START_REF] Schmeets | Afbakenen van moeilijk waarneembare bevolkingsgroepen[END_REF] however, given the specific situation of asylum seekers, overall data on migrants are unlikely to be applicable to asylum seekers.

The aim of this study is, to determine differentials in overall and cause-specific mortality between asylum seekers and the Dutch population, to relate these to the available determinants such as age, gender, and country of origin, and to identify possible subgroups at risk. Learning more about absolute number of deaths and mortality patterns may help healthcare providers plan adequate health provisions, while data about increased mortality due to specific causes of death of asylum seekers will help health authorities make choices for establishing specific prevention programmes to reduce health risks and inequalities in health.

METHODS

Study population

An asylum seeker is a person who has left his or her country of origin, has applied for recognition as a refugee in another country, and is awaiting a decision on his or her application. Referral of asylum seekers to mainstream healthcare professionals and institutions and co-ordination of care.

6

The Central Agency for the Reception of Asylum Seekers provides monthly reference data about asylum seekers in centres by age and sex, including the numbers of births, stillbirths, and deaths.

Individual data about inflow and outflow are unavailable, so we used the annual average of the monthly number of residents (listed by age group, nationality, and sex) who were present on the 1st day of each month. We summed the annual average occupations in the period 2002-2005 to obtain the denominators for our calculations.

The limited number of cases compelled us to merge countries of origin into regions (Box 2). In absence of a standard classification for health reporting for asylum seekers we used the regional classification of the United Nations High Commissioner for Refugees (UNHCR), [14] to group countries of origin. Because of the study population size, some UNHCR regions were merged on the basis of geographical location and/or cultural similarities (Appendix 1).

Box 2. Regions of origin of asylum seekers in the Netherlands

Region of origin:

Major of asylum seekers were expressed in terms of number of deaths per 1,000 or 100,000 births. These rates were compared with corresponding rates derived from the national mortality and birth registers. Mortality rates by regions of origin were compared to the mortality rates for the Netherlands by means of age and sex-stratified rate ratios. We obtained 95% confidence intervals to SMR and mortality rates using SISA's t-test procedure (http://www.quantitativeskills.com/sisa/).

For the analysis of three broad cause-of-death groups (infectious diseases, external causes, chronic diseases) by region of origin, ratios were estimated by means of Poisson regression analyses, with number of deaths as dependent variable, number of person-years at risk as offset variable, and region of origin as independent variable. The Dutch population was taken as the reference group.

The regression model was controlled for sex, and age . In the cause-specific analysis, because of small number of deaths, we applied a distinction into two broad age groups, divided in such way that the model showed the least error (e.g. 0-39 vs. 40+ years for chronic diseases). Poisson regression was applied using the R software (http://www.r-project.org). Confidence intervals were derived from the standard errors to the regression coefficients.

RESULTS

Population characteristics

The CES Europeans and ME/SW Asians were the largest subgroups of asylum seekers (table 1).

There were considerably more male than female asylum seekers, but the sex distribution differed per region (Table 1). African populations were the youngest, followed by the ME/SW Asian population. The age distribution of the CES European population was more similar to the Dutch population.

In 2002-2005, 346 asylum seekers died and 28 stillborns (in 4327 deliveries) were reported. The sex of 15 death cases was unknown, and the causes of death were unknown for 39 cases. The overall crude mortality rate (156/100,000) of this young population was lower than that of the Dutch population, which was 859/100,000 inhabitants.

Differences by age, sex, and region

Comparison of overall mortality between asylum seekers and the Dutch population showed differences between subgroups by age, sex, and region of origin (figure 1). In the age groups < 1, 1-19 and 20-39 years mortality was increased in females from WCS Africa in comparison with Dutch females. Increased mortality was also found in the age group 1-19 years for males from WCS Africa and CES Europe, and in the age group 20-39 years for females from NEH Africa and males from CES Europe. In the age groups 40-64 and 65 years and over, mortality was lower than or at the same level as in the Dutch population for all regions of origin.

Poisson regression analysis, giving standardised rate ratio's corrected for age and sex (figure 2),

shows increased risk of dying of infectious diseases for NEH and WCS Africans. WCS Africans and CES Europeans were at increased risk for dying of external causes of death, especially the young men (results not in figures). The risk of dying from chronic diseases was significantly lower in comparison with the host population for asylum seekers from all regions of origin, with exception of WCS Africa.

Mortality for subgroups of main primary cause of death categories

AIDS, hepatitis and tuberculosis are the most common causes of infectious disease deaths among both male and female asylum seekers (table 2). Out of 33 infectious disease deaths, 29 were asylum seekers from WCS and NEH of Africa. From the AIDS-related cases even 15 out of 16 originate from these regions (results not in tables).

Table 2 shows that roughly half of the non-natural deaths resulted from accidents and injuries, predominantly of male asylum seekers. Accident or injury deaths prevailed in male asylum seekers younger than 30 years (34 of 40 cases, results not in table). For accidents and injuries there appear to be differences in mortality between regions of origin but the numbers are too small to draw firm conclusions. Suicide mortality was increased in males from NEH Africa (results not in tables). The high SMR for drowning is remarkable. Drowning occurred irrespective of season, and 16 of the 20 cases were younger than 20 years (results not in tables).

DISCUSSION

This is the first study reporting overall and cause-specific mortality among asylum seekers as compared to the host population. It shows high numbers of deaths by cancer, cardiovascular diseases and external causes of death. Whereas at younger ages mortality among asylum seekers was higher than among the Dutch population, lower mortality was found above the age of 40.

Mortality from cancer and cardiovascular disease was reduced, whereas mortality due to infectious diseases, pregnancy and childbirth, and external causes was increased. Important cause of death differences between regions of origin indicate that preventive health programmes for asylum seekers require a subgroup differentiated approach.

Methodological considerations

The advantage of this study is that it provides the first data specific to asylum seekers and to identify mortality patterns within the asylum seeker population, differentiated by age, sex and region of origin. However, as a consequence of the limited size of the asylum population, although we studied four years, results for subgroups by region of origin and for cause of death categories, need to be interpreted with caution.

Part of the deaths among asylum seekers may be included in the national mortality register. They are, however, not identifiable and can therefore not be extracted from the reference data. As the number is small in comparison with the deaths in the reference population, the effect on the results is assumed to be limited.

Aggregation of data into UNHCR regions is chosen in the absence of a standard classification for asylum seekers and because of UNHCR's involvement with the study population. As the classification influences the results, validation of regional classification for health studies among asylum seekers would be welcome and would facilitate international comparison.

In the multivariate analysis, due to the limited number of cases, data were aggregated into just two age groups. This reduced error but may have allowed some effect of age differences to go unnoticed. It is unlikely that the risk differences we did find were the result of this procedure. The difference between the SMR and the rate ratio in the multivariate analysis for infectious diseases is remarkable. The SMR is very high because of the overrepresentation of younger age groups in the asylum population and because of a much higher infectious disease mortality among asylum seekers than among the Dutch in these age groups. The standardised rate ratio calculated with the Poisson regression though, is less influenced by the fact that the asylum seeker age distribution is skewed.

Results in relation to other studies

The way age affects asylum seekers' mortality, with lower mortality rates in older age groups and increased mortality rates in younger groups, is similar to that reported in labour migrant studies. [START_REF] Bos | Mortality Differences between Native Dutch and people of Turkish, Moroaccan, Surinamese, and Antillean/Aruban Origin[END_REF][START_REF] Grulich | Cancer mortality in African and Caribbean migrants in England and Wales; a follow-up study[END_REF][18][19][START_REF] Garssen | Differential mortality risks and causes of death among non-Western foreigners in the Netherlands[END_REF] The cause-specific mortality of all asylum seekers combined, matches other studies that show increased mortality from infectious diseases and external causes in migrants. [START_REF] Bos | Mortality Differences between Native Dutch and people of Turkish, Moroaccan, Surinamese, and Antillean/Aruban Origin[END_REF][START_REF] Garssen | Differential mortality risks and causes of death among non-Western foreigners in the Netherlands[END_REF][START_REF] Stirbu | Injury mortality among ethnic minority groups in the Netherlands[END_REF] Lower mortality from cancer matches other European studies among non-Western ethnic groups. [START_REF] Bos | Mortality Differences between Native Dutch and people of Turkish, Moroaccan, Surinamese, and Antillean/Aruban Origin[END_REF][START_REF] Grulich | Cancer mortality in African and Caribbean migrants in England and Wales; a follow-up study[END_REF][18][19] More importantly, we should note that analysis by region of origin showed considerable differences in mortality by causes of death between subgroups of asylum seekers.

The present study shows that increased risk of infectious disease mortality among asylum seekers is primarily a result of AIDS deaths in Africans. AIDS is, after all, a leading cause of mortality worldwide and the primary cause of death in sub-Saharan Africa.

[22] Statistics Netherlands has identified AIDS as a major cause of death for migrants. [START_REF] Garssen | Differential mortality risks and causes of death among non-Western foreigners in the Netherlands[END_REF] Tuberculosis and hepatitis are important causes of excess risk for labour migrants, [START_REF] Bos | Mortality Differences between Native Dutch and people of Turkish, Moroaccan, Surinamese, and Antillean/Aruban Origin[END_REF] but low numbers of cases in asylum seekers make it difficult to draw conclusions regarding these diseases in asylum seekers.

Infant mortality for all migrants living in the Netherlands was reported to be increased 35% in comparison with the Dutch population. [START_REF] Garssen | Differential mortality risks and causes of death among non-Western foreigners in the Netherlands[END_REF] Infant mortality among asylum seekers in this study, is similar to that of the general population. However, infant mortality is underestimated due to the fact that part of the 15 cases for which it is not reported whether the baby was alive at birth, could also be infant death cases. Perinatal mortality did not differ from the Dutch population, but was also underestimated due to underreporting of stillbirths and in addition possibly part of the 15 cases were stillbirths. The maternal mortality rate of asylum seekers was ten times as great as the general rate for the Netherlands, and twice that of the ethnic group with the highest risk (35/100,000 live births from Surinam/Antillean mothers). [START_REF] Waelput | Etniciteit en zorg rondom zwangerschap en geboorte; een verkenning van Nederlands onderzoek[END_REF] In this study, the three mothers who died of complications of pregnancy and childbirth, originated from WCS Africa, where countries have estimated maternal mortalities of 905 (453-1480)/100,000 live births. [START_REF] Hill | Estimates of maternal mortality worldwide between 1990 and 2005: an assessment of available data[END_REF] Home country risk factors for maternal mortality may still be present in women from this region. Added to the fact that WCS African asylum seekers also face many teenage pregnancies and abortions, [START_REF] Goosen | Induced abortions and teenage births among asylum seekers in the Netherlands: analysis of national surveillance data[END_REF] we believe that WCS African asylum seeker mothers and babies are at increased risk with respect to issues of reproductive health and infancy.

The increased risk among asylum seekers for accidents and injuries, adds to the occasional evidence of increased injury risks among migrant groups. [START_REF] Stirbu | Injury mortality among ethnic minority groups in the Netherlands[END_REF] Moreover, the existence of differences in injury mortality between subgroups are also seen in ethnic minority groups in the Netherlands. [START_REF] Garssen | Dalende sterfte bij autochtonen en allochtonen[END_REF] The risk of drowning among asylum seekers is twice as high as among all non-Western migrants in the Netherlands, for which a 4-8 times increased risk in comparison with the native Dutch population has been described. [START_REF] Garssen | Afname van het verdrinkingsrisico bij jonge kinderen, maar verhoogd risico bij kinderen van recent geïmmigreerde niet-westerse allochtonen[END_REF][START_REF] Van Oostrum | Afname van het verdrinkingsrisico bij jonge kinderen, maar verhoogd risico bij kinderen van recent geïmmigreerde niet-westerse allochtonen[END_REF] Suicide has been described as a risk factor for Iranians and Afghans in England, [START_REF] Cohen | Safe in our hands?: A study of suicide and self-harm in asylum seekers[END_REF] and for men from southern and eastern Europe in the Netherlands. [START_REF] Garssen | Zelfdoding onder migrantengroepen en autochtonen in Nederland. [Suicide among migrant populations and native Dutch in the Netherlands[END_REF] This study showed increased suicide mortality in males from NEH Africa. Further subgroup analysis of suicide cases, especially when data from additional years are included, may show more differences between subgroups by sex, age and region of origin, and will be studied separately. Suicide in asylum seekers may be related to traumatic events in the countries of flight and having to cope with an uncertain future. The suicide risk may also be imported from the countries of origin. Suicide rates among young men in former Soviet states have risen substantially since the 1990s, and are the major cause of death of young men. [START_REF] Shkolnikov | Changes in life expectancy in Russia in the mid-1990s[END_REF] Homicide was reported to be a risk factor for African and west Asian immigrants in the Netherlands, [START_REF] Bos | Mortality Differences between Native Dutch and people of Turkish, Moroaccan, Surinamese, and Antillean/Aruban Origin[END_REF] but was not significantly increased among the asylum population in our study.

The health advantage for older asylum seekers, particularly with regard to the major chronic diseases, has also been seen among migrants in general, [START_REF] Bos | Mortality Differences between Native Dutch and people of Turkish, Moroaccan, Surinamese, and Antillean/Aruban Origin[END_REF][START_REF] Grulich | Cancer mortality in African and Caribbean migrants in England and Wales; a follow-up study[END_REF][18][19][START_REF] Razum | Time travel with Oliver Twist. Towards an explanation for a paradoxically low mortality among recent immigrants[END_REF]33] and has been a topic of debate. The advantage may be caused by the 'healthy migrant effect', where only the strongest and healthiest in a population are able to migrate. Given the young age of many asylum seekers and the relatively older age at which the advantage is first observed, [START_REF] Uitenbroek | Life expectancy and mortality differences between migrant groups living in Amsterdam, the Netherlands[END_REF] it seems unlikely that the healthy migrant effect is an important factor in the relative health of the asylum population as a whole.

Mortality differentials between migrants and the general Dutch population diminished in the period 2002-2006, [START_REF] Garssen | Dalende sterfte bij autochtonen en allochtonen[END_REF] amongst others, influenced by acculturation. For asylum seekers such decrease is not to be expected because of the continuous influx of new asylum seekers and outflow of asylum seekers after a decision on their asylum request. Health status at immigration will therefore remain an important health determinant for natural causes of death among asylum seekers.

Implications for policy and practice

The results of our study point out important issues for asylum seeker health policies. It shows, that, in addition to the often-mentioned mental health and communicable diseases problems among asylum seekers, other health problems are of importance. The high absolute mortality for chronic diseases and external causes and the excess mortality in comparison with the host population due to infectious diseases, external causes of death and pregnancy and child birth related causes, reflects the variety of the burden of ill health among asylum seekers. It also indicates the importance of full access to health care and prevention for the asylum population. [START_REF] Norredam | Access to health care for asylum seekers in the European Union -a comparative study of country policies[END_REF] Preventive interventions should address the increased risk of subgroups for specific causes. The birth-related mortality in WCS African mothers, combined with this population's unfavourable reproductive health outcomes, [START_REF] Goosen | Induced abortions and teenage births among asylum seekers in the Netherlands: analysis of national surveillance data[END_REF] for example, indicates that targeted interventions addressing reproductive and infancy health risks, are required for this group. Drowning prevention should address all parents and children. As many asylum seekers have limited knowledge about the dangers of open water, good safety education, [START_REF] Van Oostrum | Afname van het verdrinkingsrisico bij jonge kinderen, maar verhoogd risico bij kinderen van recent geïmmigreerde niet-westerse allochtonen[END_REF] and swimming lessons should be provided.

Future research

Collection of mortality data on asylum seekers in other host countries is important as it is unclear whether the data presented can be extrapolated to asylum populations in these countries. Variations between host countries in composition of the asylum population, reception conditions, access to health care [START_REF] Norredam | Access to health care for asylum seekers in the European Union -a comparative study of country policies[END_REF], and other factors may influence asylum seeker health and consequently mortality. If mortality data for asylum seekers in other host countries become available, analysis of aggregated mortality and cause of death data from several countries could contribute to explaining risk differences between subgroups of asylum seekers. For causes of death with high relative risks but low absolute numbers, such as maternal mortality, aggregation of data from different host countries is essential to allow in depth aetiological studies.

In addition to the need for more mortality studies there is also an international need for more insight in subgroup specific morbidity. Combination of mortality and morbidity data could guide the development of screening and prevention policies and practices to reduce health risks for asylum seekers. Such policies and practices should also be based on insight into which preventive interventions work for which asylum seekers. There is serious need for studies in this domain, as prevention is an extra challenge in a population whose first concern is their asylum procedure. (2002)(2003)(2004)(2005). CES Asia and 'other countries' not presented as no satisfying regression function could be determined.

  [ 9] The study population comprises all inhabitants of asylum seeker centres in the Netherlands (Box 1). Asylum seekers live in these centres until they receive a final decision about their asylum procedure. The average duration of residence in these centres increased from[START_REF] Waelput | Etniciteit en zorg rondom zwangerschap en geboorte; een verkenning van Nederlands onderzoek[END_REF] months on 1 January 2002 to 47 months on 01 January 2005.[10] The reference population is the Dutch standard population for 2002-2005, as published by Statistics Netherlands.[11] Box 1 Health services for asylum seekers in the Netherlands in the period 2002-2005. Asylum seekers in the Netherlands live in asylum seekers centres. They have freedom of movement but they may only work a limited number of weeks annually. The Central Agency for the Reception of Asylum Seekers manages all asylum seeker centres and is responsible for the provision of several entitlements for asylum seekers, including healthcare. Asylum seekers are entitled to full access to healthcare with minor exceptions. The Central Agency for the Reception of Asylum Seekers has contracted the Community Health Services (CHS) for Asylum Seekers to provide preventive health services in all asylum seeker centres for: Health education, child healthcare, infectious disease control, hygiene and safety inspections, and specific nurse practitioner services.

Figure 1 .

 1 Figure 1. Rate ratio's by age group, sex and region of origin for asylum seekers in comparison with the Dutch standard population. 95% CIs not including 1 are considered significant. The numbers of deaths are: 0 years old (26 cases); 1-19 years old (44 cases); 20-39 years old (115 cases); 83, 40-65 years old (83 cases); 65 years and more (64 cases), 15 cases of unknown sex not included in calculations. Data available on-line (Appendix 2).

Figure 2 .

 2 Figure2. Age and sex standardised rate ratio's for disease groups per region of origin in comparison with the Dutch population. a infectious diseases; b external causes; and c chronic diseases (all primary death causes other than infectious diseases and external causes of death).(2002)(2003)(2004)(2005). CES Asia and 'other countries' not presented as no satisfying regression function could be determined.

Table 1 .

 1 Characteristics of the asylum seeker population in the Netherlands in 2002-2005

			All	WCS	NEH	CES	ME/SW	CES	Other
			asylum	Africans	Africans	Europeans	Asians	Asians	countries
			seekers
	Number of person-years
	•	Male	134,331	33,362	15,170	32,151	42,499	7,125	4,024
	•	Female	87,886	16,601	9,502	27,303	26,471	4,915	3,094
	•	Total	222,217	49.963	24,672	59,454	68,970	12,040	7,118
	Percentage of all asylum
	seekers		100	22.5	11.1	26.8	31.1	5.4	3.2
	Number of deaths*
	•	Male	193	44	21	54	59	6	10
	•	Female	138	36	13	30	36	7	16
	•	Total	346* #	80	34	84	95	13	41* ,#
	Percentage of total deaths	100	23.1	9.8	24.2	27.4	3,7	11.8
	*Nine persons whose country of origin was unknown were included in the category "other countries"

# Fifteen persons whose sex was not known are included Cause-

specific mortality: main primary cause of death categories

  The standardised overall mortality among asylum seekers was similar to that of the host population for males and females (table2). The main causes of death of asylum seekers were cancer,

	cardiovascular diseases, and external causes of death (table 2). Mortality in asylum seekers was
	significantly increased in comparison with the host population for infectious diseases; diseases of
	the blood; congenital anomalies; and external causes. In contrast, asylum seekers had lower
	mortality for cancer, cardiovascular, respiratory, gastroenterological, and neurological diseases.
	With 36 cases, perinatal mortality in asylum seekers (8.32/1000 births) was similar to that the
	Dutch population (rate ratio 1.16, 95% CI 0.84-1.61). The infant mortality rate (17 cases, 3.95/1000

live births) was not significantly different from that of the Dutch population (rate ratio 0.83, 95% CI 0.51-1.33). For 15 cases it was not reported whether the baby was alive at birth. The maternal mortality ratio (69.33/100,000 births) was 10.08 times as great as that of the Dutch population (95% CI 8.02-12.83) (results not in tables).

Table 2 . Mortality of asylum seekers as compared to the total population of the Netherlands (2002-2005): numbers of deaths, crude death rates and standardised mortality ratios

 2

	Male

* SMR standardised for age, 95% CI not including 1 in bold $ Accidents including drowning. # does not take into account the number of deliveries or births

Acknowledgements:

We thank our colleagues from the Community Health Services for Asylum Seekers for reporting mortality data. We thank the Central Agency for the Reception of Asylum Seekers for providing denominator data and Statistics Netherlands for coding the primary causes of death. We also thank A. Kunst and C. Schouten, who commented on the manuscript, and C. van Steenis and D. van der Schuit, who prepared the tables and figures. We thank Mandy Savage and Sylvia van Roosmalen for correcting the English manuscript.

Funding: Netherlands Association for Community Health Services.

Data

The Community Health Services (CHS) for Asylum Seekers have managed a unique health notification system for asylum seekers since 2002 as mortality data on asylum seekers cannot be derived from other mortality registers. Medical staff at asylum seeker centres report all deaths to their regional office. A doctor (HK) verifies and forwards the data in an anonymous form to epidemiologists at the central office of the CHS for Asylum Seekers. Statistics Netherlands codes all causes of death according to the International Classification of Diseases, 10th revision,[12] into

Competing interests: All authors declare that the answers to the questions on the BMJ competing interest form (http://bmj.com/cgi/content/full/317/7154/291/DC1) are all No and they therefore have nothing to declare.

Ethics approval: not needed.

The Corresponding Author has the right to grant on behalf of all authors and does grant on behalf of all authors, an exclusive licence (or non-exclusive for government employees) on a worldwide basis to the BMJ Publishing Group Ltd and its Licensees to permit this article (if accepted) to be published in Journal of Epidemiology and Community Health and any other BMJPGL products to exploit all subsidiary rights, as set out in our licence (http://jech.bmj.com/ifora/licence.pdf).


Zorrilla B, Galán I, Duque I, Segura Domínguez-Berjón Mf

Del Pozo

Ana Gandarillas
email: ana.gandarillas@yahoo.es

Deaths in collective dwellings and inequalities in small-area mortality: an ecological study in the Madrid region (Spain)

Keywords: Collective dwellings, Mortality, Small-Area Analysis, Socioeconomic Factors

Background: There are increasing numbers of elderly persons who reside and die in institutions, yet there are few studies that analyse the effect of this on mortality in small areas and its ensuing effect on the association between material deprivation and mortality.

Methods: Cross-sectional, ecological study in the Region of Madrid covering 3906 census tracts (median of 1000 inhabitants), using mortality data for 1996-2003, and socioeconomic deprivation from the 2001 census. Standardised mortality ratios (SMRs) were calculated for each census tract. Using the Besag-York-Mollié model, relative risks (RRs) of dying and their 95% credibility intervals (CIs) according to the deprivation index considered (with the fourth quartile, Q, being the most unfavourable situation) were calculated for deaths among: the total population; and the population excluding residents who died in institutions .

Results

A total of 6% of the deceased had been residing in institutions, that affected 16.5% of census sections (644) and accounted for 17% of the variability in SMRs among men and 10% among women, p<0.001. Mortality increased with socioeconomic deprivation, i.e., whereas the RRs for the total population in Q4 with respect to Q1 were 1.46 among men (RR 95% CI 1.41-1.50) and 1.12 among women (RR 95% CI 1.08-1.17), these figures rose to 1.48 (95% CI 1.43-1.53) and 1.14 (95% CI 1.10-1.18) respectively for the population excluding residents who died in institutions.

Conclusions

We found that deaths of residents in institutions affect variation in small-area mortality, and confound the relationship between mortality and socioeconomic deprivation. This variable should be recorded in mortality statistics so that its effect can be controlled for in subsequent analyses.

WHAT IS ALREADY KNOWN

• Geographical distribution of life expectancy and standardised mortality ratios in small-sized populations and small areas is linked to the location of nursinghomes. • No relationship has been observed between deaths in these homes in small areas and socioeconomic deprivation. • There is a need for studies that use different methodologies and target largersized populations to confirm the impact of such homes on other mortality measures.

WHAT THIS STUDY ADDS

• In a large-sized population such as that of the Madrid region (Comunidad de Madrid), this study confirms the relationship between the standardised mortality ratio in small areas and residential deaths in old age and nursinghomes, prisons, and psychiatric and geriatric hospitals ,with men and women being affected to different degrees. • The impact of old age and nursing-homes deaths, prisons, and psychiatric and geriatric hospitals on the relationship between mortality and socioeconomic deprivation is quantified. • The proportion of deaths in old age and nursing-homes, prisons, and psychiatric and geriatric hospitals, must be taken into account when it comes to interpreting small-area mortality.

Background

From a descriptive standpoint, geographical representation of a population's health status is a basic tool because it enables areas with a greater need for intervention to be identified, and planning guidelines for preventive or health-care measures to be drawn up. Furthermore, interpretation of spatial variation in any health phenomenon is useful for generation of aetiological hypotheses about the risk of falling ill. [START_REF] Elliot | Spatial epidemiology: methods and applications[END_REF] Ecological studies that analyse health status by small areas have witnessed growing interest in recent years, paralleled by the development of geographic information systems, statistical methods and software infrastructure. Nevertheless, presenting their results in a way that serves the needs of health policy makers is a problem for researchers.

(2) Such studies pose important methodological challenges. Sources of bias in spatial epidemiology are numerous and complex, and thus call for prudence in the interpretation of results. Specifically, migrations tend to result in underestimation of the effect.(3) As populations age, demand for residential care or institutional settings continues to rise. This fact is of particular interest in small-area studies, since it may give rise to excess mortality in areas with a high percentage of the population living in old people's homes, a finding that is open to misinterpretation Although its effect was described twenty years ago, (4) there are few studies which show that migration of frail individuals to long-stay residences affects geographical variation in health problems, thereby leading to a bias in estimates.(2;5-9) The indicators that have been studied are life expectancy and standardised mortality rates, though more studies are called for to examine this topic in depth, using larger-sized populations and applying different methodologies. (2;8) This study formed part of the so-called MEDEA project (socioeconomic and environmental inequalities in small areas of Spanish cities) and was aimed at quantifying the effect that deaths of residents in collective dwellings (mostly old age and nursing-homes) have on mortality rates, and its ensuing effect on the relationship between mortality and socioeconomic deprivation. Bearing in mind that 78% of the population who live in such homes are women, [START_REF]Comunidad autónoma: Madrid. Las Personas Mayores en España: Informe 2006, Datos Estadísticos Estatales y por Comunidades Autónomas[END_REF] interest attaches to studying gender-related differences.

Methods

Study design and data

This was a cross-sectional ecological study, with the units of analysis being 3906 census tracts in the Madrid region, an area having a total population of

Analysis

Standardised mortality ratios (SMRs) for each census tract, were calculated as the ratio between observed and expected deaths.Expected cases were computed, taking Spanish total mortality rates for 2001, broken down by age group and sex, as reference.

We studied the relationship between the percentage of deaths in collective dwellings and SMRs, using linear regression, calculating the coefficient of determination to estimate the variability due to this variable.

Applying the methodology of analysis proposed for the MEDEA project, ( 12) the relative risk of mortality (RRs) was calculated by quartile of the socioeconomic index, for deaths, both overall and after the exclusion of those which occurred in collective dwellings. MEDEA project used a bayesian hierarchical model, in order to reduce the extravariability involved in using SMR. Relative risks were calculated using the autoregressive conditional model developed by Besag, York and Mollié.(13) This is a Poisson spatial model with observed cases for each census tract as the dependent variable, expected cases as offset, and two random effects terms that take the following into account: the effects which vary in a structured manner in space (census tract contiguity); and a component that models the effects which vary among census tracts in an unstructured manner (census tract heterogeneity).

A conditional autoregressive model (CAR) was used for the spatial effect. The nonspatial random effect is assumed to be distributed normally with a zero mean and constant variance. This method, which is the most usual and computationally most simple, approaches the spatial dependence as an average of the spatial effect of its neighbouring areas. The areas considered are the census tracts of the region of Madrid, and the neighbouring areas are the adjacent census tracts.

For the prior distribution for the random effects for the model parameters, and the standard deviations, we chose 'vaguely' or 'weakly' informative priors distributions .In particular, a uniform distribution in a finite range (0 to 5) of the standard deviation both of the spatial random effects (spatial dependency) and the unstructured random effects (non-spatial heterogeneity). [START_REF] Barcelo | Methods to smooth mortality indicators: application to analysis of inequalities in mortality in Spanish cities [the MEDEA Project[END_REF] The deprivation index in quartiles were included in the model as explanatory variable to examine, from a a geographical and ecological point of view, its relationship with mortality.The models were fitted using Bayesian Markov chain Monte Carlo simulation methods. Posterior distributions of RRs were obtained using WinBugs 1.1.4,(14) invoked from R.(15) To this end, three Markov chains were performed, using 50000 iterations, with 10% being discarded as "burn-in" and 1 out of every 90 simulations being retained. The Brooks-Gelman-Rubin Statistic (R-hat) was used to analyse the convergence of the chains, and the effective sample size of the chains (n.eff) to control for autocorrelation. Convergence criteria were: R-hat of under 1.1; and n.eff of over 100.

RESULTS

Over the eight years of the study period (1996)(1997)(1998)(1999)(2000)(2001)(2002)(2003), 6% of the population died in collective dwellings (n=18,399), which affected 16.5% of the census sections (n=644) in the Madrid region In 30% of these (n=193), at least 20% of deaths took place in collective dwellings, which accounts for 5% of all sections. Distribution by sex and age indicated that 67% were women and 5.6% were aged under 65 years. With respect to geographical location, the greatest proportion of these deaths occurred outside the city of Madrid, and indeed, among women, this proportion was three times higher than that observed in the city (16% versus 5% respectively) (Table 1). The profile of causes of death observed in collective dwellings compared to the pattern in the general population shown that collective dwellings displayed excess mortality due to cardiovascular diseases, respiratory tract diseases, mental disorders and diseases of the nervous system (dementias), and a comparatively lower mortality due to tumours (data not shown).

Deaths in collective dwellings and standardised mortality ratio

Figure 1 depicts linear regression between the SMR and the percentage of deaths in collective dwellings, by sex. The percentage of deaths in collective dwellings accounted for 17% and 10% of the variability in mortality by census section in the total population, among men and women respectively (p<0.001).

Socioeconomic deprivation index and deaths in collective dwellings

Insofar as the relationship between the socioeconomic deprivation index and the percentage of deaths in collective dwellings was concerned, we observed an inverse and significant Pearson correlation between the two variables of: -0.10 (p=0.02) among men; and -0.12 (p=0.005) among women. The collective dwellings tend to be located in census tracts with higher income level, leading to a confounding effect between the area-level mortality and the area-level socioeconomic deprivation.

Socioeconomic deprivation index and mortality

In the case of the relationship between mortality (SMR) and the socioeconomic deprivation index, there was a positive linear association between both indicators, with a coefficient of determination among men of 9.1% for mortality in the overall population, which rose to 13% for mortality in the population excluding residents who died in collective settings (p<0.001). This association was weaker among women, 0.07% (p=0.06) in the overall population, rising to 1.4 (p<0.001) after exclusion of the group of deaths in collective dwellings (Figure 2). Table 2 shows the RRs of mortality by quartile of the deprivation index, for the population as a whole, and the population excluding residents who died in collective dwelings. Mortality was observed to rise as deprivation increased, with an excess mortality of 46% in men and 12% in women for the most underprivileged quartile visà-vis the best situation. These percentages rose to 48% and 14% respectively when deaths in collective dwellings were excluded, with an increase in the magnitude of RRs being observed across all quartiles.

Discussion

This study, undertaken in the Madrid region, quantifies the effect exerted on smallarea mortality rates by deaths of residents in collective dwellings (old age or nursinghomes in the vast majority of cases). The magnitude of mortality rates was seen to increase as the percentage of deaths in collective dwellings rose. Rather than taking place at random locations, deaths in collective dwellings in the region tended to occur predominantly outside the city of Madrid and in sections with a slightly higher economic level. Lastly, this study show the way in which this group of deaths confounds the relationship between mortality and socioeconomic deprivation, The Madrid region is fundamentally urban and economically determined by the city of Madrid, where 54% of its population lives. The geographical location of deaths in collective dwellings indicates that, among those occurring outside the city limits, women predominate, with a percentage that is three times higher than the rest of the region, i.e., 16% versus 5% respectively. The migration of older adults from the city of Madrid to old people's homes on the outskirts is also to be seen in the fact that, while 69% of the Madrid regional population dies in the city of Madrid, only 42% of all deaths in collective dwellings occur in the city.

The relationship between sections with highest mortality and those with the greatest proportion of deaths in old age homes, as well as the causal link between the two, become manifest when this relationship disappears, i.e., when the deaths of residents in collective dwellings are excluding from the analysis. This is explained by the greater frailty and the concentration of elderly in such homes. leading to a bias in the estimates. (2;5;7;8) Accordingly, the smaller the area of analysis, the greater the magnitude of this bias, with this being particularly evident in areas in which the percentage of deaths in old age homes exceeds 20% of total deaths, (7) in our particular case, 5% of all census sections. This ecological bias does not appear, however, when each unit of analysis includes the old age homes that cater for the local elderly population, thereby preventing this population's migration, such as what happens at a provincial level. (2)

The description of deaths in collective dwellings by sex and cause of death indicates a predominance of female mortality due to cardiovascular diseases and dementias, the area of mortality sure to be most affected when total deaths are included, and in such a case, special care will therefore have to be taken in interpreting small-area mortality data. Sources of bias in spatial epidemiology are numerous and complex, and prudence is thus called for in the interpretation of results. Currently, census sections are acknowledged as being the optimal geographical areas for studying spatial variability in health outcomes in cities, drawing up and evaluating health policies, and studying socioeconomic inequalities in health. (16;17) Specifically, migrations and errors in classification of exposure tend result in underestimation of the effect. In this study, control for this effect led to a discrete increase in RRs of 2% to 3%, owing to the fact that collective dwellings are found in sections with a slightly higher socioeconomic level than the rest. This association could also arise in other European regions which have large metropolitan centres that dictate their economic and population dynamic, and collective dwellings situated on the outskirts. The percentage of older adults living in collective dwellings in Spain (2.3%) is below the European mean. (18) In the Madrid region, this percentage was 2.7% in 2006. The breakdown of residential places on offer is as follows: 98.8%, old age and nursing-homes; and 1.2%, alternative accommodation systems (sheltered housing or publicfunded fostering scheme whereby families take in elderly tenants). [START_REF]Comunidad autónoma: Madrid. Las Personas Mayores en España: Informe 2006, Datos Estadísticos Estatales y por Comunidades Autónomas[END_REF] The social context of slow yet progressive ageing of the population -particularly the increase in the 80-84 and over-85 age groups, which generates a worsening in dependency factors-can be expected to lead to a notable increase in the need for residential places.(19) Accordingly, these data lead us to think that the effect of these deaths on the observed spatial mortality pattern could be intensified in the next few years and so lend this study heightened interest. Among this study's limitations is the possible underestimation of deaths in old age homes due to problems in the assigning of postal addresses and the need to use populations in family dwellings based on the 2001 census, which could result in biases in the numerator and the denominator. Furthermore, the calculated SMRs are slightly underestimated because reference rates are the total Spanish population not excluding deaths in colective dwelling. In this sense, the problem with removing the dead in collective dwellings is that rates are not comparable with the rates obtained with the entire population. Maybe its randomization by geographic units could solve both problems: the bias and the comparability. The proposed deprivation index has been constructed with data from large cities. It may not be appropriate to use the same type of indicators of deprivation in rural settings, because their meaning may be different. However, as mentioned earlier,the region of Madrid has an essentially urban nature, and only 5.8% of the population live in rural locations. Moreover, the study's cross-sectional design means that trends in the respective population groups are not taken into account.

In this regard, improvement in studies calls for a considerable investment in better data availability and quality,(3) and the usefulness of death statistics is linked to continuous improvement in quality as well as the ability to respond to new information needs.

The results of this study point to the importance of taking into account the elderly migration in the study of mortality, and the relationship between this and small-area inequalities, important question to policymakers. A variable should therefore be included in death statistics, which would enable this population group to be addressed in the analysis. In this respect, in January 2009 the Spanish National Statistics Institute approved and implemented a reform project designed to enhance the quality of death statistics.(20) This would require a record to be kept of whether the place of death was a old age home, something that, in the near future, would make it possible for mortality in this population subgroup to be analysed separately.

(13) Besag J, York J, Mollié A.

FiguresFigure 1 - 2003 Figure 2 -

 120032 Figures Figure 1 -Relationship between mortality in the total population and deaths in collective dwellings by census tracts: men and women. Region of Madrid, 1996-2003

The index accounts for more than 75% of component

	5,423,384
	(2001 Census). A census tract is a territorial unit that is fundamentally defined by
	population volume criteria and delimited by territorial features, both geographical and
	urbanistic. Its small size (median population of around 1000 inhabitants) favours
	homogeneity. The Madrid region has an essentially urban nature, with 54.2% of the
	population living in the city of Madrid and 40.0% in the surrounding Greater Madrid
	metropolitan area.
	Individual mortality data for 1996-2003 (n=305,343) were supplied by the Madrid
	Regional Statistics Institute (Instituto de Estadística de la Comunidad de Madrid).
	Based on the deceased's domicile, postal addresses were geocoded and assigned to the
	pertinent 2001 census tract. Geocoding was accurate in 95.6%, roughly approximate
	in 2.7%, and estimated in 1.7% of entries.
	Based on these data, we were able to ascertain whether the deceased resided in a
	collective or family dwelling, and create the variable, "collective", for deaths in group
	settings (old age homes, nursing-homes, prisons, and psychiatric and geriatric
	hospitals). In terms of type of collective dwelling, these were old age or nursing-
	homes in 92.4%, hospitals (geriatric or psychiatric) in 6.2%, and prisons in 1.4% of
	cases. This, in turn, enabled us to work with total deaths for the study period and, by
	extracting the deaths of residents in collective dwellings, calculate the small area
	mortality for these two populations.
	Census-tract populations, for the whole population and for residents in family
	dwellings, broken down by age group (19 groups) and sex, were drawn from the 2001
	census, the year approximately corresponding to the midpoint of the study period.
	Person-years for the period were estimated by multiplying the above populations by 8.
	Based on family-dwelling data in the 2001 population and the household census, we
	drew up indicators, and the deprivation index defined in the MEDEA Project was
	used and calculated for the Madrid region.(11)This index was calculated by principal
	components analysis, the component parts of which were: unemployment, temporary
	workers, manual workers and low educational level among both the overall adult (age
	≥16 years) and young adult (age 16-29 years) populations.

's variability. This deprivation index follows a distribution with a mean of 0 and a standard deviation of 1, in which the highest values indicate the most unfavourable situation. The quartiles of the index were calculated (with the fourth quartile being the most unfavourable situation).

Table 1 -Deceased Population in collective dwellings 1 by age, sex and geographical setting. Region of Madrid, 1996-2003 1 Colletive dwellins include old age and nursing-homes deaths prisons, and psychiatric and geriatric hospitals 2 Column percentage 3 Percentage of total deaths

 1

Table 2 -Risk of mortality by quartile of the socioeconomic deprivation index, in the total population and in the population excluding residents who died in collective dwellings.Region of Madrid, 1996-2003

 2

		Total population			Total population excluding residents who died in collective dwellings
		RRs a	95% CI	b		RRs	95% CI	b
		Men					Men
	Deprivation
	index
	Q1		1			Q1	1
	Q2		1.14	1.11 1.17	Q2	1.16	1.13 1.19
	Q3		1.27	1.23 1.31	Q3	1.29	1.25 1.33
	Q4	c	1.46	1.41 1.50	Q4	1.48	1.43 1.53
		Women				Women
	Q1		1			Q1	1
	Q2		1.02	0.99 1.06	Q2	1.03	1.00 1.06
	Q3		1.06	1.02 1.10	Q3	1.07	1.03 1.10
	Q4		1.12	1.08 1.17	Q4	1.14	1.10 1.18
	a RRs: RR deprivation (exp(β))
	b 95% CI*: 95% Credibility Interval

c Q4: quartile with greatest socioeconomic deprivation

  Bayesian Image-Restoration, with Applications in Spatial Statistics. Annals of the Institute of Statistical Mathematics 1991;43:1-20. Instituto Nacional de Estadística, Subdirección General de Censos y Padrón. Proyecto de Reforma de las Estadísticas del Movimiento Natural de la Población. 2008. "The Corresponding Author has the right to grant on behalf of all authors and does grant on behalf of all authors, an exclusive licence (or non exclusive for government employees) on a worldwide basis to the BMJ Publishing Group Ltd to permit this article (if accepted) to be published in JECH and any other BMJPGL products and sublicences such use and exploit all subsidiary rights, as set out in our licence (http://jech.bmj.com/site/about/licence.pdf)."

	(14) WinBUGS user manual. Version 1.4.1 [computer program]. Cambridge,
	MRC: 2003.
	(15) R: a language and environment for statistical computing 2006 [¡Error!
	Referencia de hipervínculo no válida. R foundation for statistical computing
	[computer program]. 2006.
	(16) Lawson AB. Statistical Methods in Spatial Epidemiology. Second ed. Yohn
	Wiley & Sons; 2006.
	(17) Krieger N, Chen JT, Waterman PD, Soobader MJ, Subramanian SV, Carson
	R. Choosing area based socioeconomic measures to monitor social inequalities
	in low birth weight and childhood lead poisoning: The Public Health
	Disparities Geocoding Project (US). J Epidemiol Community Health 2003
	Mar;57(3):186-99.
	(18) Del barrio Truchado E, Abellán García A. Indicadores Demográficos. In:
	Ministerio de Trabajo y Asuntos Sociales, Instituto de Mayores y Servicios
	Sociales (IMSERSO), Observatorio de Personas Mayores, editors. Las
	Personas Mayores en España: Informe 2006, Datos Estadísticos Estatales y
	por Comunidades Autónomas.Madrid: 2006. p. 49-94.
	(19) Servicios Sociales. In: Consejo Económico y Social, Comunidad de Madrid,
	editors. Situación Económica y Social de la Comunidad de Madrid,
	2003.Madrid: 2004. p. 547-602.
	(20)

Acknowledgements

This study formed part of the MEDEA Project (Mortality in small areas in Spain, and socio-economic and environmental inequalities), and was funded by the Ministry of Health & Consumer Affairs, Spain, (FIS: PI040069). The autors should like to thank Gonzalo López-Abente (National Center for Epidemiology, Madrid) for their statistical help and advice. Additional thanks must go to Raquel López and Dolores Núñez (Madrid Regional Statistics Institute) for suppliying the data. Finally, the autors should like to thank reviewers for the comments, that we have found very useful and informative.

Conflicts of interest: none.