Background

Perinatal health inequalities in relation to migration have been widely reported across high-income countries [1], with many studies reporting increased risks among immigrants [1, 2]. It is becoming apparent, however, that the impact of migration on perinatal health largely depends on the specific immigrant groups, on the outcome studied, and on the geographic location [1, 3]. Populations which stand out as being particularly at risk are non-European migrants to Europe, refugees and asylum-seekers, and foreign-born blacks in the U.S. [4].

In Brussels, studies have shown that mothers with a nationality from the two largest non-European immigrant groups, namely North- and Sub-Saharan Africa, experienced around 80% higher perinatal mortality rates compared to Belgians [5, 6]. Women with a Sub-Saharan African nationality were also at higher risk of giving birth preterm, whereas women from North Africa were less at risk for this outcome, compared to Belgian mothers [5, 6].

Some studies found that perinatal health inequalities between immigrant and non-immigrant populations were no longer present when adjusting for socioeconomic determinants [7, 8]. Although this effect might suggest that the socioeconomic disadvantage of immigrants might fully account for the observed inequalities in health, other studies have concluded that additional mechanisms must be at play [9, 10].

Authors have suggested that inadequate antenatal care among certain immigrant groups could be one of the key mechanisms that ought to be explored [9]. Indeed, timely antenatal care is known to prevent pregnancy complications (through screening and treatment, health advice and psychological support), it can make pregnancy a more positive experience, and can improve maternal and perinatal outcomes [11, 12]. However, studies have shown that immigrants or ethnic minorities in high-income countries may experience increased access barriers, use services less, or be more exposed to receiving suboptimal care [2, 9, 13].

Furthermore, as is the case with some perinatal health outcomes such as prematurity, the approach of comparing native women with immigrants might hide crucial differences within the immigrant population. Few studies compared the antenatal care (ANC) use between different groups of immigrants, and most were mainly carried out in North America. Findings from these studies indicated that important variations did exist, either by country of birth or by legal status [2, 13–15]. Two studies carried out in the UK showed that health-seeking behaviours were determined by socio-cultural background and familiarity with the healthcare system. The prevalence of late initiation of care varied by ethnic groups, and was highest among women of South Asian, African Caribbean, or Eastern European ethnicity born abroad. The reasons for not accessing care differed between groups: e.g., Somali and Bengali were concerned ANC would be over-medicalised, whereas Eastern European women were worried it would not be medicalised enough [16]. A French prospective study including nearly 10 000 women found that, compared to other regions of birth, women born in Sub-Saharan Africa were more likely to have inadequate antenatal care [14].

Furthermore, since socioeconomic deprivation has been associated with inadequate antenatal care on one hand [17], and given its strong link to immigration on the other hand, it seems essential that studies take into account the socioeconomic characteristics of immigrants. Such an approach enables to better understand the relationship of country of birth with the use of antenatal care, and to estimate the potential intermediate role of other determinants in this relationship.

This research investigates the associations of three birth regions (Belgium, North Africa, and Sub-Saharan Africa) with the use of antenatal care, by also considering demographic, socioeconomic and migration-related determinants.

Methods

Results

Participation rates & sample description

Our sample consisted of 932 women who fully answered the questionnaire. For 850 of these, additional clinical data was collected from hospital records. The overall participation rate was 86.4% (varying between 80.3 and 90.2% for the different nationality groups, and between 82.6 and 88.9% for the four hospitals). Our analyses concern the 879 women born in one of the three birth regions of interest.

Ninety percent of women born in North Africa were born in Morocco, 7% in Algeria, 2% in Tunisia and 1% in Lybia or Egypt. There were 20 Sub-Saharan African countries of birth, with the most represented being the Democratic Republic of Congo (31.4%), Guinea (19.6%), and Cameroon (16.0%), followed by Rwanda (5.2%), Senegal (4.7%), and Côte d’Ivoire (4.2%).

Women born in Belgium were younger, had lower parity, and experienced fewer medical complications during pregnancy than immigrant women (Table 1). Mothers born in North Africa were characterised by older age, lower education, high proportions without a professional activity, and lowest proportions in the wealthiest quartile. They were also particularly likely to have difficulties speaking the host-country languages. Mothers born in Sub-Saharan Africa had the highest proportions of grand multipara and single mothers. They were most at risk of not having their own accommodation, and poverty was prominent with almost half of women having a household income in the lowest quartile. Women from Sub-Saharan Africa were most prone to lacking health insurance, and to having an unstable legal status.

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Table 1. Demographic, clinical, and socioeconomic characteristics of women (in %), overall and by region of birth, with X² p-values.

https://doi.org/10.1371/journal.pone.0267098.t001

Antenatal care

Around half of the women in the sample were followed-up mainly by an obstetrician, and 13.2% mainly by a midwife (Table 2). The vast majority had their first antenatal consultation during the first trimester of pregnancy (93.9%), and the proportion of late initiation was distinctively higher among women born in Sub-Saharan Africa (14.4%). Among late starters, most had their first visit no later than the fourth pregnancy month, with proportions very high for women born in North Africa. The three main reasons that women cited for consulting late were, in order of prevalence: 1) not knowing that they were pregnant (44%), 2) not feeling the need to consult (16%), 3) difficulty getting an appointment earlier (12%). The reasons given by women who did not consult at all during pregnancy (n = 5) were: 1) being scared to be reported (because undocumented) and not being aware of their rights, 2) having serious family problems overtaking the priority of consulting, and 3) being in denial of pregnancy.

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Table 2. Antenatal care characteristics, overall and by region of birth, with X² p-values.

https://doi.org/10.1371/journal.pone.0267098.t002

Overall, only 5.2% of women had less than seven antenatal consultations, and 17.8% had less than the recommended number of consultations with respect to their parity. The prevalence of “infrequent consultations” was much higher in primipara (37.9%), than in multipara (6.3%). In fact, primipara having had between 7 and 9 ANC visits constituted 71% of women with “infrequent consultations”, multipara with <7 visits 22%, and primipara with less than 7 visits only 7%. Few women said that they had experienced difficulties getting an appointment or that they would have liked to have more antenatal consultations. Seven percent of women said they had had no continuity of care.

Predictors of late start of ANC.

Univariate analyses (Table 3) show that women born in Sub-Saharan Africa had almost five times higher odds of starting ANC late, compared to women born in Belgium, whereas no statistically significant difference was found for women born in North Africa.

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Table 3. Crude and adjusted odds ratios and p-values for predictors of late start of care.

https://doi.org/10.1371/journal.pone.0267098.t003

Other characteristics were identified as important predictors for late start of ANC. Of note, mothers not having their own home had 12 times higher odds of starting ANC after the first trimester compared to women who lived in private housing; and women without health insurance had 8 times higher odds. Other significant predictors of delayed start of ANC were being in the lowest income quartile, in the lowest education category, single motherhood, and having an unstable immigration status. Moreover, women who were unemployed or without a professional activity were around 4 times more likely to start ANC late than women with a job or students. Recently arrived immigrants were also more at risk of starting ANC after the first trimester, compared to women having resided in Belgium for at least 16 years.

In the multivariable model, country of birth maintained its statistically significant association with late start of care. The adjusted results showed that Sub-Saharan-born mothers had 3 times higher odds of initiating ANC late compared with non-migrants. Accommodation type and professional activity also remained strongly associated with the outcome, with women without their own home, unemployed and women without a professional activity having increased odds of initiating care late. Generally speaking, confidence intervals were large due to the small numbers of women in these categories.

Table 4 shows the prevalence of late initiation of care according to sociodemographic, socioeconomic and migration characteristics, stratified by region of birth. Among women born in Belgium, the statistically significant indicators for late start were the level of education, single motherhood, housing type, and professional activity. Among mothers born in North Africa, only age, professional activity, and health insurance status were associated with late start. However, for women born in Sub-Saharan Africa, numerous socioeconomic determinants predicted the delayed start of care: the predictors were the same as those for Belgium-born women, with the addition of health insurance and household income.

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Table 4. Predictors of late start of antenatal care by region of birth, with Chi² or Fisher exact p-values.

https://doi.org/10.1371/journal.pone.0267098.t004

Predictors of “infrequent consultations”.

Parity, housing type, and late initiation of ANC were the strongest predictors for having less than the recommended number of visits (Table 5). Despite having initiated care late, more than half (60%) of late starters born in North- and Sub-Saharan Africa had the recommended number of consultations. When adjusting for late initiation and gestation at delivery, women born in Sub-Saharan Africa were less likely to have insufficient consultations compared to women born in Belgium. The adjusted odds ratios show that primipara had 10 times higher odds of having less than the recommended number of consultations, compared to multipara. Mothers without their own accommodation had 5 times the odds compared to those in private housing. Other at-risk categories were mothers without health insurance, single mothers, and those under 25 years, those with unstable residency status, and mothers who were unemployed or dependent on social welfare or invalidity benefits.

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Table 5. Prevalence of less than recommended ANC visits, with crude and adjusted odds ratios and Wald X² p-values.

https://doi.org/10.1371/journal.pone.0267098.t005

Discussion

In summary, regardless of region of birth, the vast majority of women in this study had adequate care in terms of timing, frequency of consultations, and self-reported access. Region of birth was an independent risk factor for late initiation of care, but not for infrequent consultations. Women born in Sub-Saharan Africa were more prone to accessing care late but were not more at risk of infrequent consultations. Women born in North Africa, however, had similar adequacy of care compared to the Belgium-born population. The three groups also differed in terms of socioeconomic profiles and socioeconomic predictors of antenatal care use. Housing type, professional activity, and health insurance status were important predictors of both outcomes.

In line with population-based studies carried out in Belgium [8, 27], and with the international literature [10], our data shows that immigrant populations accumulate various dimensions of socioeconomic vulnerability. Interestingly, our results also highlight characteristic differences between the immigrant groups, such as different patterns of professional activity, housing type, lone parenthood, and immigration status, which reflect their specific migration histories, culture, and socioeconomic integration in Belgium.

Region of birth was found to be an independent risk factor for late initiation of care, but not for infrequent consultations. With some exceptions [14, 15, 28], most European studies analysed immigrant women as a single group [13], which has the limitation of masking key differences within. Our results revealed important disparities in terms of follow-up between the two groups. Indeed, women born in North Africa were not particularly at risk of late start nor of insufficient consultations, whereas women born in Sub-Saharan Africa were more likely to initiate care late, compared to native-born women. Once the first contact with healthcare professionals was established, most women from Sub-Saharan Africa appeared to receive adequate follow-up nonetheless, which indicates a responsive antenatal care system, and compliance on the patient’s part. It is possible that the high frequency of consultations despite a delayed start of care are the consequence of pregnancy complications which arose due to the lack of antenatal care in the first trimester, although additional analyses of our data offer no support for this claim. In fact, we found that the prevalence of at least one complication was 56% among women who first consulted in the first trimester, and 54% among women who consulted later.

In this respect, part of the excess adverse perinatal health outcomes described in the literature [6] for women born in Sub-Saharan Africa could potentially be due to their higher rates of delayed start of care; this is a hypothesis which should be corroborated by future studies.

Systematic reviews carried out in 2011 and 2013, found that in most included studies, ethnic minority groups or foreign-born women were more likely to initiate care late, to have fewer visits, or to have inadequate care [13, 17]. The particular vulnerability of women from Sub-Saharan African countries in terms of late initiation has been highlighted before [14, 15, 28]. When analysing potential explanatory factors, a French study concluded that women’s legal status was a greater determinant than geographic origin, with the higher proportion of inadequate care among migrants from SSA probably reflecting the higher proportion of undocumented women among them [14]. One study carried out in the Netherlands fifteen years ago found that women born in Morocco had three times the prevalence of late initiation of care compared to Dutch women [29]. Adjusting for socioeconomic and health-related factors significantly reduced, but did not eliminate the increased odds. The difference in context, timing, healthcare system, and possibly migration type are potential explanations for the discrepancy with our results.

We found a series of sociodemographic and socioeconomic factors to be associated with antenatal care, which reflects the strong impact of living conditions, poverty and health literacy on healthcare use, and possibly downplays some of the widely reported effects of ethnicity or country of origin on their own. It is crucial to remember that socioeconomic deprivation can itself be the consequence of immigration, due to the process of social exclusion [10]. We found that insufficient income, education, poor living conditions and more precarious working status were important barriers to adequate use of ANC for women born in Belgium as well as for those born in Sub-Saharan African countries. Similarly, population-based studies in Belgium had found a strong association between socioeconomic factors and perinatal health outcomes such as low birthweight and perinatal mortality in women from these two nationality groups, but not in women from North Africa [6, 27]. The impact of shorter education on healthcare use might be mediated by lower health system literacy, affecting women’s competences to access and navigate the healthcare system [30]. For instance, lack of knowledge about the healthcare structure, about eligibility, and existing services were found to be the most prevalent barrier to receiving optimal antenatal care among recent immigrants in Norway [31].

Compared to earlier studies, this is one of the few [14, 15] to include an indicator of housing type, which interestingly, appears to have a particularly strong association with both late initiation of care and infrequent visits. Our results show that the subgroup of women who lack their own accommodation are extremely at risk of having inadequate antenatal care. Secondary analyses (S2 Table) revealed that this group accumulated various socioeconomic risk factors.

The lack of healthcare coverage was a predictor for both outcomes, more strongly for late initiation of care. This indicates that the lack of health insurance is a greater barrier to initiating care than to continuing care. In fact, in Brussels, most women without health insurance at the beginning of their pregnancy are helped by healthcare professionals and collaborating social services once they have had a first contact, to gain access to health insurance, free care, or financial reimbursement, depending on their situation. Sometimes, it is more the lack of information concerning eligibility to care which hampers access, rather than the financial barrier itself. This is consistent with the experiences of some of the undocumented women in our sample who reported not initiating care because they were unaware of having cost-free and confidential access. Without any health insurance the financial costs of care could be prohibitive and the administrative procedure to obtain “Urgent Medical Care” appears unsurmountable for some [32]. Our findings highlight the necessity of ensuring that all women have the rights, the information, and logistic and financial access to a first contact with perinatal healthcare professionals, which would be more straightforward if health insurance were universal.

Regardless of region of birth, the vast majority of women in this sample received adequate antenatal care in terms of timing, frequency of consultations, and self-reported access. The prevalence of late initiation was low (6.1%), and most late starters consulted no later than the fourth pregnancy month. A study carried out in another large Belgian city in 2015 also found that 6% of women initiated care late [33], with foreign-born women being twice as exposed, compared to those born in Belgium. However, two studies carried out in Brussels in 2008 and 2016 found higher estimates. The first study was a prospective observational study of 333 women recruited in clinical centres, and found that 10.8% initiated care after 12 weeks of gestation [34]. The second was a population-based study including 11 380 low-risk pregnancies. This study found that 6.7% of women hadn’t consulted by 20 weeks of gestation [23]. Both studies excluded women with comorbidities or high-risk pregnancies, a subgroup which we can expect to be more prone to consulting early [16]. What is more, the second study also noted that the rates of late start were on a downward trend over their six-year study period (2010–2016), which suggests that the prevalence of late start might have continued to decrease thereafter. Furthermore, it should be remembered that our sample focused on three specific birth regions, which clearly represent a subset of the population and somewhat limits comparability with other studies. The rates of late initiation of ANC appear to be significantly higher in some of our neighbouring countries. Research from the UK, for instance, has estimated this prevalence at more than 30% [15, 35]. In the Netherlands it has been found to be around 10% for Dutch women, and higher for ethnic minorities such as Moroccan (30%) [28, 29]. A study carried out in Norway this year found that 16% of recent immigrants consulted after the first trimester, although only 2.5% initiated care after week 21 [31]. A recent study carried out in France, also found higher estimates of women consulting past the first trimester: 14% for non-migrants, 19% for legal migrants, 30% for undocumented migrants [14]. Thus, in comparison to these observations, the initiation of antenatal care in Brussels appears to be exceptionally good. Increasingly, non-profit organisations in Brussels help pregnant women access healthcare and offer psychosocial support [36–38], which could partly explain the improving and overall adequate antenatal care use. The estimate of late initiation of ANC used in our analyses was based on self-reported timing. If we used the timing extracted from clinical records instead, the prevalence increased to 10%. We can be quite certain that this latter figure is an overestimation given that 29% of mothers had at least part of their follow-up outside of the hospital where the data was extracted, meaning that the first consultation appearing in the hospital software (which we extracted) was not their first one. When we calculated late initiation using clinical data except when women were partly followed-up elsewhere, we found an estimate of 6.7%, which only slightly exceeds the self-reported one. We can thus be rather confident that the true measure lies around 6–7%, and certainly no more than 10%.

Most late starters consulted just a few weeks into their second trimester, and only 15% of them reported having had difficulties getting an appointment. What is more, the main reasons that women gave for initiating care late were the delayed recognition of pregnancy and the lack of perceived need to consult in the first trimester. These findings indicate that the late initiation of care was not predominantly due to access barriers such as lack of legal access, difficulty navigating the system or getting an appointment, but often due to a lack of perceived need. These are certainly not the sole mechanisms, but they do suggest that ensuing courses of action aimed at improving adequacy of ANC and reducing inequalities, should include the following: facilitate women’s recognition of early pregnancy; ensure adequate access to pregnancy tests or diagnosis by a clinician; and improve women’s (and their partners’) awareness of the importance of early initiation of care.

It is conceivable that public health interventions increasing awareness about the importance of starting ANC in the first trimester could shift the initiation of care forward by a few weeks. This would be all the more relevant given that the women most prone to initiating care late appear to be those who might benefit most from a timely start. In fact, antenatal care not only serves to enhance physical health, but is also an entry door into social and psychological support, which can be particularly valuable to women living in socioeconomic deprivation. The fact that delayed initiation of care was the strongest predictor of insufficient consultations is certainly not surprising, but it underlines, yet again, the importance of a timely start.

Overall, very few women revealed having had difficulties getting an appointment (4%) or wishing to have had more visits (7%). However, a high proportion (17.8%) had received less than the 10 visits recommended for primipara and the 7 for multipara. This high prevalence was mainly driven by primipara having attended between 7 and 9 antenatal visits. Whether having one or a few consultations less than what is recommended should be considered “inadequate” is subject to debate; the WHO, for instance, considers 8 antenatal visits to be adequate [39]. Indeed, other studies have used lower thresholds of inadequate care, e.g. less than 50% of recommended visits [14], no care, or less than 3, 4, or 7 consultations [13]. Furthermore, when we measured the proportion of primipara having attended less than 10 consultations in clinical records, we found it to be slightly lower than that reported by women (10% vs. 14%), thus it is possible that we have slightly overestimated the prevalence of women having had less than the recommended number of visits.

One of the strengths of this study concerns the inclusion of a series of individual-level indicators which cannot be obtained through routine data (e.g., legal status, income, housing type, difficulty accessing ANC, reasons for consulting late). The inclusion of three particular nationality groups was deliberate and has allowed us to explore their specificities. Furthermore, the administration of the questionnaire via face-to-face interviews and the use of interviewers speaking the most prevalent languages allowed us to obtain a high participation rate, minimising selection bias and missing data.

One limitation of this study is that there were few participants in the most at-risk categories, such as women without their own accommodation or women without health insurance. This, together with the low prevalence of late initiation of care, limited the statistical power, yielding large confidence intervals and preventing us to carry out multivariable models stratified by country of birth. Future studies purposefully including larger numbers of women with the most precarious profiles could overcome these limitations. Furthermore, despite our efforts to avoid excluding mothers, we were not able to include roughly 1% due to language barriers, and 1.8% who were too unwell to participate (due to illness or exhaustion). However, these low percentages preclude any significant impact on the generalisability of the study. We must also recognise that in the same way that analysing region of birth groups separately enabled us to discern important differences, we could be missing further crucial variations within each of these groups. For instance, Sub-Saharan African countries include a vast spectrum of realities in terms of socioeconomic contexts, culture, and types of migration.

In order to assess the generalisability of this study, we have compared some of the sociodemographic characteristics of the included participants with complete population data of women having given birth in Brussels between 2005–2010 [27]. Bearing in mind that the population data precedes our data collection, and that it is limited to singleton births, we find that the relative differences between the three groups are comparable (e.g. highest proportion of primipara among women born in Belgium, followed by women born in Sub-Saharan Africa; highest percentage of single motherhood among Sub-Saharan African mothers and lowest among North African; proportion of women with university degree highest among women born in Belgium and lowest among those born in North-Africa). However, in our sample we included fewer very young mothers and more highly educated mothers, compared to the overall birth population. Although this tendency is common among research study participants, it somewhat limits the generalisability of the study.

Finally, we would like to underline the existence of numerous models of antenatal care, and the lack of agreement on best practice, including care provider type, number of visits and continuity of care [40, 41]. In this study, we have relied on the national Belgian guidelines to assess the adequacy of initiation and frequency of care. Furter research to identify the most adequate antenatal care pathways would be valuable, not only to improve maternal and neonatal outcomes, but also to enable meaningful international comparisons on healthcare use.

Conclusions

The large majority of women in this study had adequate care in terms of timing, frequency of consultations, and self-reported access, regardless of their country of origin. In most cases, delayed start of care was due to a lack of perceived need, rather than to administrative, financial, or logistic access barriers.

The three region of birth groups differed in terms of socioeconomic profiles, use of antenatal care, and in terms of socioeconomic predictors of ANC use. Women born in Sub-Saharan Africa were more prone to accessing care late but were not more at risk of having infrequent consultations. Women born in North Africa, on the other hand, had similar adequacy of care compared to the Belgium-born population.

The inequalities in ANC use were mainly related to few but highly discriminating socioeconomic determinants, such as housing type, professional activity, and health insurance status.

Future research into migrants’ use of ANC should therefore continue to take into account their place of birth and socioeconomic characteristics. Furthermore, additional dimensions of adequacy of care, such as quality and content of care, could provide useful additional insights.

Based on our findings, we recommend three types of policies to improve equitable access and utilisation of healthcare: 1) increasing early uptake of ANC by improving timely recognition and testing of pregnancy, and by raising awareness on the importance of care in the first trimester, 2) improving immigrant women’s socioeconomic integration, and 3) universalising the access to public health insurance, which in Belgium would mean removing the logistic barrier of applying for “Urgent Medical Care”.

Supporting information

Acknowledgments

We express our gratitude to all study participants, and to the heads of obstetrics and neonatal services of CHU Brugmann, CHU St Pierre, Erasme and Iris-Sud Ixelles hospitals for giving us permission to carry out the study. We also thank hospital staff (midwives and gynaecologists) for the logistic support in recruiting mothers and accessing clinical data. We are also grateful to the members of the steering committee, including Dr Barlow and Professor Godin, for guiding the design of this research. We would also like to thank the interviewers.