Table 2 shows that mothers from Morocco (naturalised and not naturalised) have significantly fewer low birth weight babies and fewer preterm babies than Belgian mothers (p < 0.0001). The same is true for mothers from Turkey, who also have significantly fewer low birth weight babies than Belgians. This difference is particularly striking for naturalised Turkish mothers (p = 0.001). In contrast, a significantly higher risk of preterm birth was observed for mothers from sub-Saharan Africa (naturalised and not naturalised) compared to Belgian-born mothers (p < 0.05).
We observed a significantly greater proportion of low Apgar scores among non-naturalised mothers from Morocco and sub-Saharan Africa compared to Belgians (p < 0.0001). Conversely, among Turkish naturalised mothers the rate is significantly lower than for Belgians.
3.3. Perinatal mortality according to nationality
Mortality rates vary widely according to nationality (Table 2). Babies of mothers who have the same nationality at their own birth and at delivery, from Morocco, sub-Saharan Africa and Turkey experience a striking excess of perinatal mortality (p < 0.0001 compared to Belgians). For the same three origins, however, when mothers have adopted Belgian nationality, perinatal mortality is similar to Belgian-born mothers.
Table 3 shows the results of the logistic regression analyses. There is no significant interaction between nationality and the number of incomes from declared employment, parity, multiple births and mother's age. Adjusting for multiple births, mother's age and parity had a small impact on the odds ratio for sub-Saharan women (not shown). The adjustment for the number of parents with an income slightly decreases the OR for babies of mothers from Morocco and Turkey. In contrast, the perinatal mortality rate for babies of mothers from sub-Saharan Africa is no longer significantly different to the Belgian rate, after adjustment. For Moroccan and sub-Saharan African naturalised mothers the crude and adjusted OR for perinatal mortality is not significantly different compared to the Belgians. For Turkish naturalised mothers the adjusted OR for perinatal mortality is lower than for Belgian mothers (p < 0.001).
3.4. Perinatal death by causes
Compared to Belgians, perinatal deaths by all causes except immaturity were significantly higher for babies of Moroccan mothers (Table 3). Mothers from Turkey experience a significant excess of perinatal mortality by congenital anomalies, asphyxia and unexplained death prior to the onset of labour and immaturity compared to Belgian mothers. Among mothers from sub-Saharan Africa, only mortality from asphyxia and unexplained death prior to onset of labour and from conditions consequent upon immaturity are significantly increased compared to Belgian mothers. Adjustment for age of the mother, parity, multiple births, and number of incomes in the household do not substantially change the findings. For Moroccan, sub-Saharan African and Turkish naturalised mothers, none of the crude and adjusted OR for perinatal causes of death was significantly different from that for Belgian mothers.
4. Comment
4.1. Perinatal mortality among immigrants
This study confirms that the association between nationality at mother's birth and birth outcomes is not uniform but depends on the migrant subgroup [1] and [10]. As observed in our previous study, the excess of perinatal mortality for sub-Saharan mothers is mainly explained by an excess of preterm birth, low birth weight and a low socio-economic level [2]. The excess of mortality by conditions consequent upon immaturity among sub-Saharan African mothers may be linked to the high rate of preterm birth. This may in turn be explained by a higher incidence of hypertension, diabetes and infection and has been widely discussed in our previous work [2]. Other studies indicate that sub-Saharan African origins are positively associated with adverse perinatal outcomes [4] and [11].
This study observed a similar pattern for Turkish and Moroccan mothers. Similar results have shown a higher rate of perinatal death by congenital anomalies among Moroccan and Turkish mothers [12], [13], and [14]. This increased rate of death from congenital anomalies may be related to two components: on the one hand, marriage between cousins or between people who come from close communities, and on the other hand, differences in utilisation of antenatal screening services. For migrant populations, Stoltenberg et al. [15] show a twice higher risk of congenital malformations among children whose parents were first cousins in Norway. For differentials in utilisation of screening services, and also presumably in choice of pregnancy termination in the case of major congenital anomaly, this has also been described in France [16]. The excess of perinatal mortality due to congenital anomalies does not persist after naturalisation, presumably due to change of behaviour.
4.2. Adequate access to and utilisation of (perinatal) health care services
A further component of the differences between perinatal outcomes among migrants may be cultural differences, such as lifestyle factors (nutrition, folic acid), and poor use of prenatal care [2]. Several studies from different countries suggest that the increased risk of other adverse perinatal outcomes is associated with late or inadequate prenatal and obstetric care due to the difficulty in accessing public health services [17].
One of the important differences among maternal risk groups is their access to preventive health care during the prenatal period. Mothers who acquire Belgian nationality may be more familiar with the language, the health care system and other relevant aspects of the host society. Indeed, cultural and linguistic barriers may limit access to health services during pregnancy and the lack of cultural mediators in prenatal clinics may lead to inequalities in pregnancy surveillance, especially for new immigrants [18]. Increasing participation in a host society is related to more health services utilisation, and language ability appears to play a central role in the uptake of health care and on the effect on pregnancy outcomes [19].
4.3. Proxy measure of acculturation (naturalised Belgian citizens)
In our study, we observe a favourable effect of naturalisation on birth outcomes and perinatal mortality for Moroccan, Turkish and sub-Saharan African mothers. Our results follow up on the study of Cacciani et al. [4] showing that migrant status is a risk factor for adverse perinatal health but the adverse outcomes decrease over time among immigrants. They suggest improvement policies are adopted, in order to increase accessibility to mother–child health services. Bollini et al. [3] have also suggested that integration policy is an important determinant of birth outcomes in migrant populations. In this study, Belgium is categorised as a country with permissive integration policies where steps are taken to acknowledge cultural differences and specific needs in order to facilitate the entry of new immigrants.
Nevertheless, birth outcomes may either improve or deteriorate with duration of residence, depending on the migrant group [1]. Troe et al. [20] have shown that among Turkish mothers in the Netherlands, infant mortality as well as perinatal and congenital causes of death increase with lower age at immigration. This trend, however, completely differs among the Surinamese migrants, suggesting a better integration in Dutch society, with adequate access and utilisation of perinatal health care.
In our study, Moroccan, Turkish and sub-Saharan African mothers may be similar to the Surinamese in the Netherlands, due to their integration in the host country. A common explanation for this integration is the acculturation theory, which is a multidimensional phenomenon that has different effects on pregnancy outcomes and nationality [19]. In our study, our proxy measure of acculturation (naturalisation) is not associated with a decrease in protective cultural behaviours among Moroccan and Turkish mothers but with a decrease in perinatal mortality. Health outcomes of immigrants tend to converge towards the level observed in the host population, presumably via changes in health-related behaviours. More particularly, acculturation is associated with the use of general practitioner care among Turkish and Moroccan migrants in the Netherlands [21]. It is also associated with significant changes in health behaviour, health and morbidity for ethnic minority groups [22].
4.4. Limitations of the study
Contrary to the mother's nationality at delivery, we observed a large number of missing data for nationality at mother's own birth (29.8%). Nevertheless, nationality percentages are consistent with data from CEPIp in Brussels in 2008 [23] and missing data are mainly Belgian mothers. There is some evidence that when the family is Belgian, the category “nationality of origin” is not always filled in. Our results may also be biased by misclassification. Autopsies are rarely conducted among migrants [24], which could lead to a possible overestimation of the number of cases of unexplained deaths that occur prior to the onset of labour, as well as an underestimation in the other causes of death categories.
Because of the >30% missing value for the education and occupation variables derived mainly from death certificates, and to avoid bias, we used the number of incomes within the household as an indicator of the socioeconomic level. This indicator has been validated in the evaluation of precarious situations [25] but it is not a complete indicator of the socioeconomic level. We also have to be careful in our interpretation of the OR value in the categories “intrapartum events” and “conditions consequent upon immaturity” because there were few subjects and the large 95% confidence interval limits our statistical interpretation. Finally, an important item of data which would be very useful in order to study acculturation is the duration of stay of migrants.
5. Conclusion
Perinatal mortality and causes of perinatal deaths vary according to nationality in Brussels but the excess of perinatal mortality for Moroccan, sub-Saharan African and Turkish mothers does not persist after adopting Belgian nationality. The demographic trajectories of immigration, acculturation and use of health services or cultural contexts are probably different according to the mothers’ nationalities.
Acknowledgement
We thank Ms. Emmanuelle Rivière for editing the manuscript.
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Footnotes
a CR Epidemiology, Biostatistic and Clinical Research, School of Public Health, Free University of Brussels, Brussels, Belgium
b Health and Social Observatory of Brussels, Brussels, Belgium
Corresponding author at: CR Epidemiology, Biostatistic and Clinical Research, School of Public Health, Free University of Brussels, CP598, Route de Lennik 808, 1070 Brussels, Belgium. Tel.: +32 2 555 40 47; fax: +32 2 555 40 49.