Abstract
Background and Aims:
Gestational diabetes is more common in many first-generation immigrant women in Europe and other Western countries. Less is known about second-generation immigrant women; such knowledge is needed to understand generational influences on diabetes risk. We aimed to study second-generation immigrant women regarding the presence of all types of diabetes during pregnancy.
Methods and Results:
A cohort study was conducted using the Swedish National Birth Register, the National Patient Register, and the Total Population Register. We used Cox regression analysis to compute hazard ratios (HRs) and 99% confidence intervals (99% CI) for any diabetes during pregnancy and specific subtypes (gestational diabetes, pre-existing diabetes type 1, pre-existing diabetes type 2) in second-generation immigrant women compared with Swedish-born women with two Swedish-born parents while adjusting for sociodemographic factors, family history of diabetes, body mass index, smoking habits, and comorbidities. The study population included a total of 989,986 deliveries and 17,938 diabetes cases. The fully adjusted HR (with 99% CI) for any type of diabetes during pregnancy among second-generation immigrant women was 1.11 (1.05–1.18). Higher risks were found in women with parents from Africa, Asia, or Eastern Europe, as well as Denmark. A lower risk for pre-existing type 1 diabetes was found overall and for women with parents from most geographic regions.
Conclusion:
In this national cohort study, the risk of all types of diabetes during pregnancy was increased in second-generation immigrant women. Diabetes prevention and treatment is especially important in these women both before and during pregnancy.
Keywords: Diabetes, Gestational diabetes, Immigrant women, socioeconomic factors
Background
Diabetes is increasing globally [1], in parallel with the obesity epidemic [2]. The prevalence of diabetes worldwide was estimated to be 9% in men and 8% in women in 2013 [1]. Gestational diabetes is also increasing in prevalence and affects nearly 20 million births each year globally [3]. In addition, gestational diabetes is a risk factor for later onset of type 2 diabetes [4–6], and also for cardiovascular diseases among women [7]. Furthermore, gestational diabetes is often preventable, and identification of high-risk groups could thus help target preventive interventions where they are most needed. One possible high-risk group is immigrant women, who may need more support to eat a healthier diet and to be physically active during pregnancy [8, 9], as well as after delivery.
Diabetes mellitus type 2 is more common in some immigrant groups in Europe. In the UK, a higher prevalence of diabetes, mostly type 2, has been reported in immigrants from South Asia compared to the native-born British population since the 1980s [10, 11]; and in the Netherlands, a higher prevalence of diabetes, mostly type 2, has been described in immigrants from Turkey and Morocco [12]. In Sweden, the prevalence of diabetes has been found to be higher in immigrants from non-European countries, especially in women [13, 14].
A review found an increased risk of gestational diabetes among almost all immigrant groups in Western countries and especially in Europe [15]. A higher risk of gestational diabetes among immigrant women has been reported in several studies from Norway [16–18], and Denmark [19]. We recently found a higher risk of all types of diabetes during pregnancy in first-generation immigrant (i.e. foreign-born) women in Sweden, particularly for gestational diabetes and pre-existing type 2 diabetes [20]. Low socioeconomic status has also been found to be associated with a higher risk of gestational diabetes [21], as well as with cardiovascular health in general [22], which may confound positive associations in immigrant populations. Having access to national register data in Sweden has made it possible to study gestational diabetes in all pregnant women, and also to link country or region of origin of the parents for almost all second-generation immigrants.
The aim of this study was to examine the risk of diabetes among pregnant second-generation immigrant women, including both pre-existing diabetes and gestational diabetes. Studies of second-generation immigrant women are of particular interest as they represent a growing part of the female population in many European countries. In addition, second-generation immigrants may often adopt a different type of lifestyle (such as diet and physical activity) than their parents and, subsequently, face different types of health hazards than the first generation. The results of this study may therefore improve our understanding of generational influences on diabetes risk in pregnancy and help guide prevention and treatment strategies in high-risk subgroups of women.
Methods
2.1. Design
We used several national Swedish registers to construct the present cohorts: the Swedish Medical Birth Register (MBR) with data on all deliveries in Sweden, the Swedish Total Population Register (TPR), and the Swedish National Patient Register (NPR). These registers are maintained by Statistics Sweden and the Swedish National Board of Health and Welfare, and include data on births, deaths, marital status, family relationships, and migration to Sweden. The completeness of the Swedish TPR is high, with the inclusion of practically 100% of births and deaths, 95% of immigrations and 91% of emigrations [23]. The NPR contains all diagnoses reported from hospitals and inpatient hospital care from all of Sweden since 1987, with a proportion of missing data of 0.9%, and with more than 99% of all somatic and psychiatric hospital discharges being registered [24]. For out-patient hospital care, diagnoses were included nationwide from 2001 and onwards from specialist care, and the rate of missing data has been estimated to be 3% [25]. The follow-up period of the present study ran from January 1, 1998 until delivery, death, emigration, or the end of the study period on December 31, 2018, whichever came first. We included all women with a recorded delivery in the MBR. Second-generation immigrants were defined as women born in Sweden with at least one foreign-born parent, and the comparison group consisted of Swedish-born women with two Swedish-born parents.
2.2. Inclusion criteria
We included all diagnoses of diabetes during pregnancy (with ICD codes), i.e. Diabetes mellitus in pregnancy (O24), including the following groups: 1. Diabetes mellitus arising in pregnancy (O24.4), 2. Pre-existing diabetes mellitus, insulin-dependent (O24.0), 3. Pre-existing diabetes mellitus, noninsulin-dependent (O24.1), and 4. Other types of diabetes including pre-existing malnutrition-related diabetes mellitus (O24.2), pre-existing diabetes mellitus, unspecified (O24.3), and Diabetes mellitus in pregnancy, unspecified (O24.9).
2.3. Covariates
We included family history of diabetes among at least one parent or sibling, body mass index (BMI), and smoking habits.
2.4. Comorbidities
We included maternal hypertension, also including pre-eclampsia and eclampsia (O10-O16), hyperlipidemia (E78), and all cancer types (C00-C97) as these variables could act as potential confounders.
2.5. Demographic and socioeconomic variables
Age was used as a continuous variable in the analysis.
Educational attainment was categorized as ≤9 years (partial or complete compulsory schooling), 10–12 years (partial or complete secondary schooling) and >12 years (attendance at college and/or university).
Geographic region of residence was included in order to adjust for possible regional differences in health care and was categorized as (1) large cities, (2) southern Sweden and (3) northern Sweden. Large cities were defined as municipalities with a population of >200,000 and comprised the three largest cities in Sweden: Stockholm, Gothenburg and Malmö.
2.6. Neighborhood deprivation
We used a neighborhood deprivation index, which was derived from Small Area Market Statistics (SAMS). The average population in each SAMS neighborhood is approximately 2000 people for Stockholm and 1000 people for the rest of Sweden [26]. A summary index was calculated to characterize neighborhood-level deprivation that was categorized into four groups: more than one standard deviation (SD) below the mean (low deprivation level or high socioeconomic status (SES)), within one SD of the mean (moderate deprivation level or moderate SES) (used as reference group), more than one SD above the mean (high deprivation level or low SES), or unknown neighborhood deprivation level/SES [27].
2.7. Statistics
Baseline data are presented with categorical variables as counts and percentages. We used Cox regression analysis to estimate hazard ratios (HR) and 99% confidence intervals (99% CI) for diabetes during pregnancy in different groups of second-generation immigrant women (compared to Swedish-born women with two Swedish-born parents) during the follow-up period. Three models were used: Model 1 adjusted for age and region of residence in Sweden; Model 2 adjusted for age, region of residence, educational level, marital status, and neighborhood SES; Model 3 adjusted for the variables in Model 2 and family history of diabetes, BMI, and relevant comorbidities. Furthermore, we conducted sub-analyses that stratified diabetes into four groups, i.e. gestational diabetes, pre-existing type 1 diabetes, pre-existing type 2 diabetes, and other forms of diabetes.
Results
In total, 989,986 deliveries were recorded in the study population, with 17,938 cases of diabetes during pregnancy (Table 1). Regarding background factors, higher educational levels were associated with a lower risk of diabetes, and living in more deprived neighborhoods was associated with a higher risk of diabetes (Table 2). Having hyperlipidemia, BMI ≥25 kg/m2, or a family history of diabetes was associated with a higher risk of diabetes during pregnancy.
Table 1.
Baseline characteristics and number of diabetes cases in Swedish-born women with two Swedish-born parents and second-generation immigrant women.
| Women with two Swedish-born parents | Second-generation immigrant women* | |||||||
|---|---|---|---|---|---|---|---|---|
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| Population | Diabetes | Population | Diabetes | |||||
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| No. | % | No | % | No. | % | No | % | |
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| Total population | 818776 | 14218 | 171210 | 3720 | ||||
| Age (years) | ||||||||
| <20 | 8133 | 1.0 | 142 | 1.0 | 3399 | 2.0 | 76 | 2.0 |
| 20–29 | 364745 | 44.5 | 5868 | 41.3 | 83601 | 48.8 | 1728 | 46.5 |
| 30–39 | 413904 | 50.6 | 7383 | 51.9 | 77842 | 45.5 | 1713 | 46.0 |
| 40+ | 31994 | 3.9 | 825 | 5.8 | 6368 | 3.7 | 203 | 5.5 |
| Educational level | ||||||||
| ≤ 9 | 170106 | 20.8 | 3525 | 24.8 | 53363 | 31.2 | 1337 | 35.9 |
| 10–12 | 404911 | 49.5 | 7253 | 51.0 | 74226 | 43.4 | 1571 | 42.2 |
| > 12 | 243759 | 29.8 | 3440 | 24.2 | 43621 | 25.5 | 812 | 21.8 |
| Region of residence | ||||||||
| Large cities | 380550 | 46.5 | 6551 | 46.1 | 97030 | 56.7 | 2050 | 55.1 |
| Southern Sweden | 288322 | 35.2 | 5016 | 35.3 | 47739 | 27.9 | 1026 | 27.6 |
| Northern Sweden | 149904 | 18.3 | 2651 | 18.6 | 26441 | 15.4 | 644 | 17.3 |
| Neighborhood deprivation | ||||||||
| Low | 203040 | 24.8 | 2786 | 19.6 | 31237 | 18.2 | 440 | 11.8 |
| Middle | 506383 | 61.8 | 8959 | 63.0 | 80687 | 47.1 | 1697 | 45.6 |
| High | 108311 | 13.2 | 2457 | 17.3 | 50360 | 29.4 | 1333 | 35.8 |
| Unknown | 1042 | 0.1 | 16 | 0.1 | 8926 | 5.2 | 250 | 6.7 |
| Smoking history | ||||||||
| Non-smoking | 712822 | 87.1 | 12058 | 84.8 | 143735 | 84.0 | 3015 | 81.0 |
| Yes | 69024 | 8.4 | 1515 | 10.7 | 20178 | 11.8 | 541 | 14.5 |
| Unknown | 36930 | 4.5 | 645 | 4.5 | 7297 | 4.3 | 164 | 4.4 |
| Body mass index, kg/m2 | ||||||||
| <18.5 | 15421 | 1.9 | 131 | 0.9 | 4204 | 2.5 | 47 | 1.3 |
| 18.5–24.9 | 461307 | 56.3 | 5068 | 35.6 | 93534 | 54.6 | 1204 | 32.4 |
| 25–29.9 | 178884 | 21.8 | 3768 | 26.5 | 38424 | 22.4 | 1023 | 27.5 |
| >30 | 80595 | 9.8 | 3859 | 27.1 | 18390 | 10.7 | 1096 | 29.5 |
| Unknown | 82569 | 10.1 | 1392 | 9.8 | 16658 | 9.7 | 350 | 9.4 |
| Family history of diabetes | ||||||||
| No | 671359 | 82.0 | 8809 | 62.0 | 131131 | 76.6 | 1998 | 53.7 |
| Yes | 147417 | 18.0 | 5409 | 38.0 | 40079 | 23.4 | 1722 | 46.3 |
| Diagnosis of cancer | ||||||||
| No | 787260 | 96.2 | 13687 | 96.3 | 165895 | 96.9 | 3584 | 96.3 |
| Yes | 31516 | 3.8 | 531 | 3.7 | 5315 | 3.1 | 136 | 3.7 |
| Diagnosis of maternal hypertension | ||||||||
| No | 816329 | 99.7 | 14133 | 99.4 | 170800 | 99.8 | 3702 | 99.5 |
| Yes | 2447 | 0.3 | 85 | 0.6 | 410 | 0.2 | 18 | 0.5 |
| Diagnosis of hyperlipidemia | ||||||||
| No | 815866 | 99.6 | 13431 | 94.5 | 170620 | 99.7 | 3566 | 95.9 |
| Yes | 2910 | 0.4 | 787 | 5.5 | 590 | 0.3 | 154 | 4.1 |
Women born in Sweden who had at least one foreign-born parent.
Table 2.
Associations between baseline characteristics and any diabetes during pregnancy in Swedish-born women with two Swedish-born parents and second-generation immigrant women.*
| Women with Swedish-born parents | Second-generation immigrant women** | |||||
|---|---|---|---|---|---|---|
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| HR | 99% CI | HR | 99% CI | |||
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| Birth year | 0.99 | 0.99 | 1.00 | 0.99 | 0.98 | 0.99 |
| Educational level (ref. ≤ 9) | ||||||
| 10–12 | 0.90 | 0.85 | 0.95 | 0.94 | 0.84 | 1.06 |
| > 12 | 0.84 | 0.78 | 0.90 | 0.97 | 0.84 | 1.11 |
| Region of residence (ref. Large cities) | ||||||
| Southern Sweden | 0.94 | 0.89 | 0.99 | 0.97 | 0.87 | 1.09 |
| Northern Sweden | 0.94 | 0.88 | 1.00 | 1.04 | 0.88 | 1.21 |
| Neighborhood deprivation (ref. Low) | ||||||
| Middle | 1.14 | 1.07 | 1.22 | 1.35 | 1.15 | 1.57 |
| High | 1.31 | 1.21 | 1.42 | 1.64 | 1.39 | 1.92 |
| Unknown | 1.06 | 0.52 | 2.17 | 1.92 | 1.44 | 2.56 |
| Diagnosis of cancer (ref. Non) | 0.95 | 0.84 | 1.08 | 1.17 | 0.91 | 1.50 |
| Diagnosis of maternal hypertension (ref. Non) | 1.26 | 0.92 | 1.72 | 1.47 | 0.75 | 2.89 |
| Diagnosis of hyperlipidemia (ref. No) | 13.60 | 12.22 | 15.13 | 10.68 | 8.41 | 13.57 |
| Family history of diabetes (ref. No) | 2.39 | 2.27 | 2.51 | 2.42 | 2.20 | 2.66 |
| Smoking history (ref. No) | ||||||
| Yes | 0.97 | 0.89 | 1.05 | 1.03 | 0.90 | 1.18 |
| Unknown | 1.07 | 0.93 | 1.22 | 1.14 | 0.87 | 1.49 |
| Body mass index, kg/m2 (ref. 18.5–24.9) | ||||||
| <18.5 | 0.79 | 0.61 | 1.01 | 0.88 | 0.58 | 1.35 |
| 25–29.9 | 1.76 | 1.65 | 1.87 | 1.89 | 1.68 | 2.14 |
| >30 | 3.65 | 3.43 | 3.89 | 4.02 | 3.56 | 4.54 |
| Unknown | 1.38 | 1.25 | 1.53 | 1.48 | 1.21 | 1.81 |
Fully adjusted. Bold values denote statistical significance
Women born in Sweden who had at least one foreign-born parent.
The relative risk of diabetes during pregnancy among second-generation women is shown in Table 3. Overall, the risk of diabetes was increased (Model 3: HR, 1.11; 99% CI, 1.05–1.18), and particularly in women with at least one parent from Denmark, Eastern Europe (in particular women from former Yugoslavia), Africa, and Asia (in particular Lebanon and Iraq, but also other Asian countries outside the Middle East region).
Table 3.
Incidence of gestational diabetes in female second-generation immigrants vs female Swedish-born individuals expressed as hazard ratios (HR) with 99% confidence intervals (99% CI)
| Model 1 | Model 2 | Model 3 | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Obs. | HR | 99% CI | HR | 99% CI | HR | 99% CI | ||||
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| Sweden | 14218 | 1 | 1 | 1 | ||||||
| All with foreign-born parent(s) | 3720 | 1.29 | 1.23 | 1.36 | 1.18 | 1.12 | 1.25 | 1.11 | 1.05 | 1.18 |
| Nordic countries | 1500 | 1.20 | 1.11 | 1.30 | 1.14 | 1.06 | 1.23 | 1.09 | 1.01 | 1.17 |
| Denmark | 248 | 1.50 | 1.25 | 1.80 | 1.41 | 1.17 | 1.69 | 1.37 | 1.14 | 1.64 |
| Finland | 1059 | 1.14 | 1.04 | 1.25 | 1.09 | 0.99 | 1.19 | 1.03 | 0.94 | 1.12 |
| Iceland | 12 | 1.27 | 0.56 | 2.88 | 1.27 | 0.56 | 2.90 | 1.41 | 0.62 | 3.20 |
| Norway | 181 | 1.22 | 0.98 | 1.51 | 1.16 | 0.94 | 1.43 | 1.14 | 0.92 | 1.41 |
| Southern Europe | 121 | 0.97 | 0.75 | 1.26 | 0.94 | 0.72 | 1.22 | 0.92 | 0.71 | 1.19 |
| France | 12 | 0.82 | 0.36 | 1.87 | 0.87 | 0.38 | 1.99 | 0.93 | 0.41 | 2.11 |
| Greece | 42 | 1.06 | 0.68 | 1.65 | 0.97 | 0.63 | 1.51 | 0.96 | 0.62 | 1.49 |
| Italy | 26 | 0.85 | 0.48 | 1.48 | 0.84 | 0.48 | 1.46 | 0.77 | 0.44 | 1.35 |
| Spain | 24 | 1.00 | 0.56 | 1.79 | 0.98 | 0.55 | 1.76 | 0.99 | 0.55 | 1.77 |
| Other Southern Europe | 17 | 1.10 | 0.55 | 2.20 | 1.04 | 0.52 | 2.08 | 0.96 | 0.48 | 1.92 |
| Western Europe | 175 | 0.81 | 0.66 | 1.01 | 0.83 | 0.67 | 1.03 | 0.84 | 0.68 | 1.04 |
| The Netherlands | 14 | 0.89 | 0.42 | 1.92 | 0.93 | 0.43 | 1.99 | 0.88 | 0.41 | 1.89 |
| UK and Ireland | 2 | 0.87 | 0.12 | 6.54 | 0.97 | 0.13 | 7.27 | 0.97 | 0.13 | 7.31 |
| Germany | 130 | 0.82 | 0.64 | 1.06 | 0.84 | 0.65 | 1.08 | 0.84 | 0.66 | 1.08 |
| Austria | 21 | 0.70 | 0.38 | 1.31 | 0.72 | 0.39 | 1.34 | 0.75 | 0.40 | 1.39 |
| Other Western Europe | 8 | 0.87 | 0.32 | 2.39 | 0.93 | 0.34 | 2.55 | 1.01 | 0.37 | 2.76 |
| Eastern Europe | 513 | 1.45 | 1.27 | 1.65 | 1.28 | 1.12 | 1.46 | 1.24 | 1.09 | 1.41 |
| Bosnia | 99 | 1.17 | 0.87 | 1.55 | 1.03 | 0.77 | 1.37 | 1.06 | 0.79 | 1.41 |
| Yugoslavia | 359 | 1.60 | 1.37 | 1.86 | 1.42 | 1.22 | 1.66 | 1.34 | 1.15 | 1.56 |
| Croatia | 9 | 0.81 | 0.31 | 2.09 | 0.74 | 0.29 | 1.91 | 0.80 | 0.31 | 2.07 |
| Romania | 23 | 1.26 | 0.69 | 2.28 | 1.21 | 0.67 | 2.20 | 1.13 | 0.62 | 2.04 |
| Bulgaria | 7 | 0.92 | 0.31 | 2.70 | 0.84 | 0.29 | 2.46 | 0.80 | 0.27 | 2.34 |
| Other Eastern Europe | 16 | 2.07 | 1.01 | 4.21 | 1.75 | 0.85 | 3.58 | 1.58 | 0.77 | 3.24 |
| Baltic countries | 32 | 0.83 | 0.50 | 1.37 | 0.88 | 0.53 | 1.46 | 0.94 | 0.56 | 1.55 |
| Estonia | 31 | 0.96 | 0.58 | 1.61 | 1.04 | 0.62 | 1.73 | 1.09 | 0.65 | 1.82 |
| Latvia | 1 | 0.16 | 0.01 | 2.69 | 0.16 | 0.01 | 2.79 | 0.18 | 0.01 | 2.99 |
| Central Europe | 172 | 1.13 | 0.91 | 1.41 | 1.12 | 0.90 | 1.40 | 1.08 | 0.87 | 1.34 |
| Poland | 100 | 1.19 | 0.89 | 1.58 | 1.16 | 0.87 | 1.55 | 1.13 | 0.85 | 1.51 |
| Other Central Europe | 17 | 0.80 | 0.40 | 1.59 | 0.83 | 0.42 | 1.66 | 0.84 | 0.42 | 1.67 |
| Hungary | 55 | 1.20 | 0.82 | 1.76 | 1.19 | 0.81 | 1.75 | 1.09 | 0.74 | 1.60 |
| Africa | 149 | 1.84 | 1.45 | 2.33 | 1.68 | 1.32 | 2.13 | 1.39 | 1.09 | 1.76 |
| Northern America | 25 | 0.75 | 0.42 | 1.32 | 0.80 | 0.45 | 1.42 | 0.82 | 0.46 | 1.45 |
| Latin America | 118 | 1.17 | 0.90 | 1.52 | 1.05 | 0.81 | 1.37 | 0.94 | 0.72 | 1.22 |
| Chile | 80 | 1.17 | 0.85 | 1.61 | 1.02 | 0.74 | 1.40 | 0.85 | 0.62 | 1.17 |
| South America | 38 | 1.17 | 0.74 | 1.86 | 1.14 | 0.72 | 1.82 | 1.19 | 0.75 | 1.89 |
| Asia | 888 | 1.78 | 1.61 | 1.96 | 1.48 | 1.33 | 1.65 | 1.30 | 1.17 | 1.45 |
| Turkey | 182 | 1.33 | 1.08 | 1.65 | 1.06 | 0.85 | 1.32 | 0.94 | 0.76 | 1.17 |
| Lebanon | 117 | 2.06 | 1.58 | 2.68 | 1.64 | 1.26 | 2.15 | 1.32 | 1.01 | 1.72 |
| Iran | 88 | 1.38 | 1.02 | 1.87 | 1.31 | 0.96 | 1.78 | 1.21 | 0.89 | 1.64 |
| Iraq | 218 | 2.06 | 1.69 | 2.51 | 1.73 | 1.38 | 2.17 | 1.38 | 1.10 | 1.73 |
| Other Asia countries | 283 | 2.08 | 1.75 | 2.47 | 1.83 | 1.53 | 2.18 | 1.74 | 1.46 | 2.07 |
| Russia | 11 | 0.80 | 0.34 | 1.89 | 0.79 | 0.33 | 1.87 | 0.84 | 0.36 | 1.99 |
Model 1: adjusted for age and region of residence in Sweden; model 2: adjusted for age, region of residence in Sweden, educational level, marital status, and neighborhood deprivations; model 3: model 2 + comorbidities, smoking, body mass index, and family history of diabetes.
Bold values are statistically significant at a significance level of 0.01.
The specific types of diabetes during pregnancy in second-generation immigrant women are shown in Table 4. The risk of gestational diabetes was increased among second-generation immigrant women overall (HR, 1.27; 99% CI, 1.19–1.36). For different regions, the risk was increased in women whose parents originated from Eastern Europe, Central Europe, Africa, or Asia. The risk of pre-existing type 1 diabetes was lower among second-generation immigrant women overall (HR, 0.72; 99% CI, 0.64–0.82), and in women whose parents were from countries in Southern, Western, and Eastern Europe, Latin America, or Asia. For pre-existing type 2 diabetes, the risk did not reach statistical significance (HR 1.33; 99% CI, 0.98–1.82), but did so in women whose parents were from Asia. For other types of diabetes, the overall risk was higher, and for certain regions in women whose parents originated from Eastern Europe or Asia.
Table 4.
Fully adjusted hazard ratios (HR) and 99% confidence intervals (99% CI) for diabetes during pregnancy in second-generation immigrants vs Swedish-born women with two Swedish-born parents, stratified by different types of diabetes*.
| Gestational diabetes | Pre-existing type 1 diabetes | Pre-existing type 2 diabetes | Other types of diabetes | |||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
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| Obs. | HR | 99% CI | Obs. | HR | 99% CI | Obs. | HR | 99% CI | Obs. | HR | 99% CI | |||||
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| Sweden | 8808 | 1 | 4356 | 1 | 388 | 1 | 666 | 1 | ||||||||
| All with foreign-born parents | 2686 | 1.27 | 1.19 | 1.36 | 679 | 0.72 | 0.64 | 0.82 | 123 | 1.33 | 0.98 | 1.82 | 232 | 1.32 | 1.04 | 1.67 |
| Nordic countries | 956 | 1.09 | 0.99 | 1.20 | 419 | 1.05 | 0.90 | 1.21 | 50 | 1.25 | 0.82 | 1.93 | 75 | 1.21 | 0.85 | 1.71 |
| Southern Europe | 92 | 1.13 | 0.84 | 1.52 | 21 | 0.52 | 0.28 | 0.98 | 4 | 1.14 | 0.27 | 4.79 | 4 | 0.67 | 0.16 | 2.82 |
| Western Europe | 131 | 0.99 | 0.77 | 1.28 | 34 | 0.56 | 0.34 | 0.91 | 2 | 0.35 | 0.05 | 2.66 | 8 | 0.98 | 0.35 | 2.70 |
| Eastern Europe | 417 | 1.66 | 1.43 | 1.92 | 41 | 0.33 | 0.21 | 0.51 | 15 | 1.42 | 0.66 | 3.05 | 40 | 1.70 | 1.05 | 2.75 |
| Baltic countries | 21 | 0.94 | 0.51 | 1.76 | 10 | 0.99 | 0.40 | 2.44 | 0 | 1 | 0.96 | 0.06 | 16.71 | |||
| Central Europe | 128 | 1.33 | 1.03 | 1.72 | 34 | 0.67 | 0.41 | 1.09 | 3 | 0.69 | 0.13 | 3.59 | 7 | 0.93 | 0.31 | 2.74 |
| Africa | 108 | 1.62 | 1.22 | 2.14 | 22 | 0.73 | 0.40 | 1.35 | 7 | 2.47 | 0.82 | 7.45 | 12 | 1.63 | 0.70 | 3.82 |
| North America | 17 | 0.93 | 0.46 | 1.85 | 7 | 0.68 | 0.23 | 2.00 | 1 | 1.33 | 0.08 | 23.13 | 0 | |||
| Latin America | 97 | 1.20 | 0.90 | 1.61 | 13 | 0.38 | 0.17 | 0.84 | 3 | 0.89 | 0.17 | 4.69 | 5 | 0.69 | 0.19 | 2.48 |
| Asia | 699 | 1.68 | 1.49 | 1.91 | 73 | 0.37 | 0.26 | 0.53 | 37 | 2.19 | 1.27 | 3.76 | 79 | 1.84 | 1.23 | 2.73 |
| Russia | 5 | 0.62 | 0.17 | 2.23 | 4 | 1.03 | 0.25 | 4.30 | 1 | 3.26 | 0.19 | 56.68 | 1 | 1.40 | 0.08 | 24.50 |
Fully adjusted (adjusted for age, region of residence in Sweden, educational level, marital status, neighborhood deprivations, comorbidities, smoking, family history of diabetes, and body mass index). Bold values denote statistical significance
Discussion
The main findings of this study were that the overall risk of diabetes during pregnancy was increased in second-generation immigrant women compared to Swedish-born women with two Swedish-born parents. The risk was especially high in women with parent(s) from Africa and Asia, but also from some European countries, such as Denmark and former Yugoslavia.
Prior studies have reported increased risks of gestational diabetes among almost all immigrant groups that were evaluated, mostly among immigrants to Western countries and especially in Europe [15]. This was also shown in other Nordic countries, including Norway [16–18], and Denmark [19], and in Sweden for some immigrant women from non-European countries, especially in the Middle East [13, 14, 20]. The present study shows that the patterns for second-generation immigrant women were similar to those previously reported for first-generation immigrants, but with lower risk magnitudes. For example, the overall adjusted HR for any diabetes in pregnancy was 1.18 (99% CI 1.12–1.25) in the present study, compared with 1.69 (99% CI 1.61–1.78) previously reported in first-generation immigrant women (p<0.001 for difference in HRs) [20]. A surprising finding was the higher risk in women whose family originated from Denmark, which currently remains unexplained. Low socioeconomic status has also been associated with a higher risk of gestational diabetes [21]; this is consistent with the findings in the present study.
Furthermore, we examined different types of diabetes during pregnancy. As a result of low numbers in various subgroups, we reported most results by regions rather than specific countries. Although the number of women with pre-existing type 2 diabetes was relatively low, the patterns of risks were similar to those for gestational diabetes, which was expected. The patterns for pre-existing type 1 diabetes showed quite different results, with lower risks found in second-generation immigrant women. As type 1 diabetes has a high prevalence among children in Nordic countries [28], especially Sweden and Finland, this finding was not surprising. A higher risk in immigrant women originating from Finland could also have been expected, but it is possible that women with pre-existing type 1 diabetes were less likely to emigrate, i.e., a “healthy migrant effect” wherein those who emigrate tend to have better health than people from their country of origin [29].
There are limitations to our study. We used register-based data and were unable to confirm the underlying criteria for the reported diagnoses. Thus, we could not categorize “other types of diabetes” in more detail, even if we suspect that most were type 2 diabetes. However, the Swedish national registers have been shown to be of high standard and validity [23, 24, 30].
In conclusion, second-generation immigrant women had elevated risks of diabetes during pregnancy, but with lower risk magnitudes than those recently reported by us for first-generation immigrant women [31], thus reflecting the importance of environmental influences on diabetes risk in these populations. Second-generation immigrant women had increased risks of both gestational diabetes and pre-existing type 2 diabetes. These elevated risks across multiple generations in immigrant families call for increased awareness and tailored prevention of diabetes during pregnancy in Sweden, which is currently not part of routine clinical practice. Diabetes prevention and treatment may be especially important in immigrant women both before, after and during pregnancy.
Acknowledgements
We thank Patrick O’Reilly for language editing.
Funding
This work was supported by the National Heart, Lung, and Blood Institute at the National Institutes of Health [R01 HL139536 to C.C. and K.S.] as well as funding from
The Swedish Research Council and The Swedish Heart Lung Foundation to Kristina Sundquist.
Footnotes
Compliance with Ethical Standards
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent was not applicable, as the study was based on pseudonymized data from registers. Research data are not shared.
The study was approved by the Regional Ethical Review Board in Lund (ref nr 2008/471 and later amendments).
Conflict of Interest
The authors have no conflict of interest to report.
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