Abstract
Background:
Although racial/ethnic disparities in neonatal and infant health are well known, positive associations between migration and perinatal health exist among immigrant mothers in western countries. There are unique marriage migration, East Asia culture, universal national health insurance system, and adequate social support in Taiwan that may differ from the situation in western countries. We aimed to assess the neonatal outcomes among live births to married immigrant mothers in recent years in Taiwan.
Methods:
We conducted a population-based analysis among all the live births in Taiwan during the period 1998–2003 to assess neonatal outcomes, including incidence of low birth weight and preterm birth and of early and late neonatal mortality, according to maternal nationality. Logistic regression was used to estimate the odds ratios (ORs) associated with low birth weight and preterm birth, and Cox proportional hazards were used to estimate the relative risks (RRs) associated with mortality in the neonatal period.
Results:
There were a total of 1,405,931 single live births, including 6.6% born to immigrant mothers and 93.4% born to Taiwanese mothers. Disparities existed among the intercultural couples, including paternal age, parental educational level, and residential distribution. Fewer low birth weight and fewer preterm babies were born to immigrant mothers than to Taiwanese mothers. In addition, babies born to immigrant mothers had lower early neonatal and neonatal mortalities than those born to Taiwanese mothers. There were lower risks of having a low birth weight (adjusted OR [AOR] 0.73, 95% confidence interval [CI] 0.70-0.75) or preterm (AOR 0.72, 95% CI 0.69-0.74) baby and lower hazard ratios (HRs) of having an early neonatal death (adjusted HR [AHR] 0.68, 95% CI 0.56-0.82) or neonatal death (AHR 0.74, 95% CI 0.64-0.87) in babies born to immigrant mothers. There is a gradual increase in the risks of adverse neonatal outcomes associated with increases in length of residence.
Conclusions:
Evidence of a healthy immigrant mother effect on neonatal health is clear. Despite lower parental education, advancing paternal age, and spatial distribution disparity, babies born to married immigrant mothers in Taiwan had favorable neonatal outcomes.
Introduction
Racial/ethnic disparities in neonatal and infant health are well known. During the last two decades, positive associations between migration and perinatal health exist among so-called high-risk immigrant mothers in western countries. 1,2 Despite many demographic and socioeconomic risk factors among Mexican-origin Latina women, these minority ethnic mothers demonstrate a similar risk of low birth weight and a lower risk of infant mortality compared with white women in the United States. 1 Similarly, in Belgium, infants born to North African immigrants with increased maternal risk factors have been reported to have higher birth weights than infants of Belgian origin. 2 Proposed explanations for the epidemiologic observations include complex immigration selection processes, cultural protective factors, and levels of social support. 3,4 In recent years, there has been an increase in the Asian Indian population accompanying the growth of the high-technology industry in the United States. 5 These new immigrant women seemingly have a lower sociodemographic risk because of better prenatal care, low rates of teenage pregnancy, and higher levels of education, yet these women have a higher incidence of low birth weight and fetal mortality than U.S.-born white women. 5 Current research that consider that foreign-born status may confer a protective effect or pose a threat on neonatal outcomes across different racial/cultural groups provides limited explanation for these epidemiologic observations. 3 –6
Marriage immigration in Taiwan has just emerged in recent years and is supported through government policies and marriage brokers. Many women from poverty-stricken countries have decided to become marriage immigrants because of their economic situation. 7 The proportion of intercultural couples, who have relatively lower socioeconomic status (SES) and educational levels, has increased in Taiwan from 15.7% in 1998 to 32.1% in 2003. In parallel to this increase, the proportion of neonates born live to intercultural parents increased substantially from 5.1% in 1998 to 13.4% in 2003, corresponding to an almost 3-fold increase. 8 Most mothers among these intercultural couples were new immigrants from mainland China, Vietnam, Indonesia, Cambodia, or Thailand. Notably, most marriages between a Taiwanese man and a foreign spouse occur to fulfill the heritage ideal, meaning that women are expected to give birth to a son to carry on the man's family name and bloodline. 9 Yang and Wang's study 10 showed that married immigrant women fulfill Taiwanese family expectations and usually become pregnant within 6 months of their wedding.
Racial/ethnic disparities in neonatal and infant health are well known, and an epidemiologic paradox exists among immigrant mothers in western countries. In Taiwan, unique marriage migration, East Asia culture, universal national health insurance system, and adequate social support differ from the situation in western countries. Consequently, we conducted a population-based analysis of all the live births in Taiwan during the period 1998–2003 to assess neonatal outcomes among those born to married immigrant mothers.
Materials and Methods
Sources of data
We used birth certificate registration data from the Ministry of the Interior in Taiwan containing information about birth outcomes and potential risk factors. The Children Welfare Act, 11 implemented in October 1994, requires birth notification to be completed by an obstetrician or midwife within 10 days of a live birth. The form contains the following information: parental nationality, national identification numbers, dates of birth, education, marital status, residential county and town, neonatal identification number, date of birth, birth weight, gestational age, parity, single or multiple birth, and information about the hospital or clinic and the obstetrician or midwife.
Death certificate registration data are maintained by the Department of Health in Taiwan. All death certificates issued in Taiwan have been computerized since 1971 and include national identification number, date of birth and death, education, residential county and town, and underlying cause of death. The underlying cause of death is systematically coded according to the ninth revision of the International Classification of Diseases.
Study population
There were 1,596,498 live births registered in Taiwan between 1998 and 2003. We excluded live births outside Taiwan by excluding infants whose registered dates were 3 months later than their birthday (n=37,678, 2.4%). Analysis was restricted to single births because of the complexity of factors influencing neonatal outcomes in multiple pregnancies 12 and to women aged ≥20 years because of the complexity of factors influencing neonatal outcomes for younger mothers. 13 We also excluded immigrant fathers to more accurately explore the immigrant mother effect only. After excluding births for mothers<20 years (n=28,404, 1.8%), nonsingle births (n=39,153, 2.5%), immigrant fathers (n=3,417, 0.2%), and all observations for which the covariates of interest were missing (n=81,915, 5.1%), a total of 1,405,931 (88.1%) live births were entered into the study. Each neonatal identification number was linked with death certificate registration data from the Department of Health of Taiwan.
Definitions of married immigrant mothers
In order to study birth outcomes and neonatal deaths among married immigrant mothers, we used those born to Taiwanese mothers as a comparison group. Immigrants may acquire alien or permanent resident certificates (80.6% and 19.4 % between 1987 and 2005, respectively 14 ). We further classified immigrant mothers according to their length of residence in Taiwan: <12 months, 12–23 months, 24–35 months, and ≥3 years. We used the date of registration for marriage as an approximation of the time of immigration. Taiwanese mothers are defined as those who may have been born in Taiwan and have Taiwanese nationality.
Definitions of birth outcomes and neonatal deaths
Low birth weight refers to babies with birth weight <2,500 g, and preterm birth refers to babies born before 37 completed weeks (259 days) of gestation, as measured from the first day of the last menstrual period. Neonatal death refers to deaths among live births during the first 28 completed days of life. This may be subdivided into early neonatal deaths, occurring during the first 7 days of life, and late neonatal deaths, occurring after the seventh day but before 28 completed days of life. 15
Statistical analysis
We used chi-square tests to compare maternal nationality (immigrant and Taiwanese) with parental characteristics and neonatal outcomes, including low birth weight and preterm birth, and mortality rates of early neonatal, late neonatal, and neonatal deaths. Logistic regression models were used to estimate crude and adjusted odds ratios (ORs) and 95% confidence intervals (CIs) of birth outcomes. Cox proportional hazard models were used to estimate crude and adjusted hazard ratios (HRs) and 95% CIs of neonatal deaths according to maternal nationality. We examined and adjusted for several risk factors for birth outcomes and neonatal deaths, which potentially confound the relationship between maternal nationality and birth outcomes and neonatal mortality. Maternal age (20–24, 25–29, 30–34, and ≥35 years), paternal age (<30, 30–34, 35–39, and ≥40 years), maternal-paternal age difference (≤−10, −9–−5, −4–0, and ≥1 year), parental education (≤6, 7–9, 10–12, and ≥13 years), maternal-paternal educational difference (≤−4, −3–0, 1–4, and ≥4 years), residential area (rural, suburban, urban), parity (primipara, multipara), and infant sex (male, female) were taken into account in the models for low birth weight and preterm birth and early neonatal and neonatal mortalities. Finally, we focused on liveborn children to primiparous mothers to explore the immigrant mother effect in terms of length of residence in Taiwan. We analyzed the data using the SAS 8.02 package (Carey, NC).
Results
Table 1 shows parental characteristics and neonatal outcomes of live births according to maternal nationality, immigrant (n=93,161, 6.6%) and Taiwanese (n=1,312,770, 93.4%). Compared to Taiwanese mothers, immigrant mothers were younger, had lower educational levels, and were more primiparous, whereas their husbands were older and also lower in educational levels. A higher proportion of these couples resided in rural areas. In maternal-paternal age and educational differences, 52.7% of Taiwanese mothers and 4.5% of immigrant mothers were 10 years younger than their husbands, and 19.1% immigrant mothers and 6.7% of Taiwanese mothers had 4 more educational years than their husbands. There were fewer male, fewer low birth weight, and fewer preterm babies born to immigrant mothers than to Taiwanese mothers. In addition, babies born to immigrant mothers had less early neonatal and neonatal mortalities than Taiwanese mothers, whereas there was no significant difference in late neonatal mortality between them.
Based on chi-square tests.
Maternal-paternal age difference was calculated as maternal −paternal age.
Maternal-paternal educational difference was calculated as maternal − paternal educational years.
Table 2 shows crude odds or HRs for neonatal outcomes of live births for immigrant vs. Taiwanese mothers. There were significantly lower risks of having a low birth weight (OR 0.88, 95% CI 0.86-0.91) or preterm (OR 0.76, 95% CI 0.73-0.78) baby among immigrant mothers. Similarly, there were significantly lower HRs of having an early neonatal (HR 0.77, 95% CI 0.64-0.91) or neonatal (HR 0.84, 95% CI 0.73-0.96) death in babies born to immigrant mothers. After adjusting for parental characteristics and infant sex (Table 3), there were lower risks of having a low birth weight (adjusted OR [AOR] 0.73, 95% CI 0.70-0.75) or preterm (AOR 0.72, 95% CI 0.69-0.74) baby, and lower HRs of having an early neonatal (AHR 0.68, 95% CI 0.56-0.82) or neonatal (AHR 0.74, 95% CI 0.64-0.87) death in babies born to immigrant mothers.
Reference category.
Maternal-paternal age difference was calculated as maternal − paternal age.
Maternal-paternal educational difference was calculated as maternal − paternal educational year.
CI, confidence interval; HR, hazard ratio; OR, odds ratio.
Adjusted for all variables in the table.
Reference category.
Maternal-paternal age difference was calculated as maternal−paternal age.
Maternal-paternal educational difference was calculated as maternal−paternal educational year.
Table 4 shows the immigrant mother effect in terms of length of residence in liveborn children to primiparous mothers only. There was a significantly low risk of having a low birth weight (AOR 0.76, 95% CI 0.72-0.79) or preterm (AOR 0.67, 95% CI 0.64-0.70) baby and of having an early neonatal (AHR 0.61, 95% CI 0.46-0.82) or neonatal (AHR 0.70, 95% CI 0.56-0.87) death in babies born to immigrant mothers with length of residence <12 months. There is a gradual increase in the risks of adverse neonatal outcomes associated with increases in length of residence.
Reference category: Taiwanese primiparous mothers.
Adjusted for maternal age, maternal-paternal age difference, paternal education, maternal-paternal educational difference, residential area, and infant sex.
Discussion
Our findings show that despite lower parental education levels, advancing paternal age, and uneven residential location patterns, babies born to married immigrant mothers in Taiwan have favorable neonatal outcomes, including lower incidence of low birth weight, preterm birth, and early neonatal and neonatal mortality rates. Despite these positive associations, potential risks or protective factors must be addressed before making further inferences.
It is widely accepted that the risk of adverse perinatal outcomes increases for infants born to mothers who have immigrated from lower-income countries because of low SES, lower educational levels, inequity of prenatal care, and minimum awareness and knowledge of meeting the complex social and cultural construction of childbirth. 16,17 Our study demonstrates disparities in parental education, advancing paternal age, and residential distribution among intercultural parents. Accordingly, these disparities may increase the risk of adverse perinatal outcomes. There are some characteristics among these married immigrant mothers that have a potentially advantageous influence, however. Mothers who have immigrated to Taiwan for marriage may selectively have chosen favorable conditions for healthy conception and delivery. Our results show that these mothers were younger and had lower rates of advancing maternal age compared with their Taiwanese counterparts. Moreover, maternal factors, such as younger age and a lower rate of advancing maternal age, in immigrant mothers may decrease the use of fertility drugs and assisted reproductive techniques and, consequently, decrease rates of low birth weight and preterm birth and neonatal mortality.
We found that higher maternal-paternal educational differences are associated with a reduction in low birth weight, preterm birth, and even early neonatal mortality after adjusting for paternal education and other risk factors (Table 3). Our results also show that immigrant mothers had higher rates of higher maternal-paternal educational differences compared with their Taiwanese counterparts; this observation could be crucial. Parental education level in Taiwan is a better socioeconomic indicator when examining birth outcomes than is occupation or family income. 18 It is well known that low parental SES is associated with poor perinatal outcomes through intermediate factors, such as poor maternal nutrition, inadequate health-related behaviors, or insufficient access to prenatal care. Moreover, maternal status plays a more important role than paternal status in determining the outcome of pregnancy. 19 Therefore, we tentatively conclude that high maternal-paternal educational differences may reduce adverse perinatal outcomes, especially for those fathers with low education levels.
Immigrant mothers may also engage in more effective health-related behaviors. For instance, in a Taiwan birth cohort pilot study, 20 the prevalence of breastfeeding initiation for Taiwanese mothers was higher than for those of immigrant mothers. Among mothers who initiated breast feeding, however, a fewer proportion of infants born to Taiwanese mothers was still breastfed at the age of 6 months. Employed Taiwanese mothers weaned earlier than others, and unemployed immigrant mothers breastfed longest. Moreover, Taiwanese families' high expectations of a married immigrant woman's fertility and the government's free provision of prenatal examinations as part of the National Health Insurance system might be important factors contributing to the majority of immigrant mothers attending early prenatal examination. 21 Thus, the favorable neonatal outcomes can be partly explained by such.
Some unfavorable factors should also be considered, however. Parental age discordance is an important marker for complex socioeconomic conditions. Parental age difference has been identified as a risk factor for adverse perinatal outcomes, such as fetal death, prematurity, and small for gestational age births. 22 There were unusual age differences among intercultural couples in our study. We found that mothers who were 10 years younger than their spouses had an increased risk of low birth weight, preterm birth, and even neonatal mortality (Table 3). The role of parental age discordance on perinatal outcome should not be overlooked. Furthermore, the level of urbanization was an important determinant of infant death rate; urban areas had much lower rates than rural areas in Taiwan. 23 There was a higher proportion of intercultural couples residing in rural areas, where possible socioeconomic disparity or inadequacy of prenatal and neonatal intensive care exists, and this could also be linked to higher risks for adverse perinatal outcomes (Table 3).
Our study demonstrates that there was a gradual increase in risks for adverse neonatal outcomes along with an increase in length of residence. Recently, healthy immigrant effects were proposed to underscore the importance of nongenetic determinants of maternal health. 24 Similarly, Ray et al. 25 explored the relationship between immigration to Canada and the risk of obstetric complications, including preeclampsia and eclampsia, placental abruption, and placental infarction. There was a progressively lower risk of maternal obstetric complications associated with how recently mothers had immigrated. Proposed explanations for this epidemiologic observation among immigrant mothers in western countries include complex immigration selection processes, cultural protective factors, and social support. 3,4 Although there are apparent differences in the purpose of migration, cultural background, healthcare systems, and social support between Taiwan and western countries, our study demonstrates similar results. We suggest that young, educated, healthy, and potentially fertile brides have favorable neonatal outcomes.
Our findings are subject to several limitations similar to findings of other retrospective cohort studies. The use of live births as the study population may overlook both spontaneous abortions and stillbirths and, thus, create selection bias. For example, if immigrant mothers have more spontaneous abortions and stillbirths, fetuses that survive live birth may be stronger and healthier than those born to Taiwanese mothers; that is, weaker fetuses from immigrant mothers could have died before the time points measured in this study. Although there is no abortion registration system in Taiwan, the stillbirth rates in immigrant and Taiwanese mothers were 6.0‰ and 9.3‰, respectively, in 2003. 26 The fact that stillbirth rates in immigrant mothers were lower than those among Taiwanese mothers refutes the argument that immigrant mothers have more spontaneous abortions and stillbirths.
Another selection bias may be our restriction to single live births to mothers over the age of 20. Before the exclusions, however, there were even larger differences between rates of low birth weight, preterm births, and early neonatal and neonatal mortalities in neonates born to immigrant mothers compared to those of Taiwanese mothers (5.8 vs. 7.0%, 6.1 vs. 8.1%, 1.6‰ vs. 2.3%, and 2.5% vs. 3.3%, respectively). These discrepancies came mainly from fewer teenage pregnancies, no pregnancies outside marriage, and fewer multiple pregnancies in neonates born to immigrant mothers. Thus, underestimation could have occurred in this study.
Gould et al. 27 reported that there was a striking relationship between incomplete birth certificates and both neonatal and postneonatal mortality in the United States. Underreported variables in birth certificates and underregistration of infant deaths, particularly those occurring during the early neonatal period, could affect the completeness of vital statistics of infants in Taiwan before 1994. 28 Fortunately, complete implementation of the revised birth registration system from October 1994, according to the Children Welfare Act, 11 requires the obstetrician or midwife to provide birth information to household and health authorities within 7 days of childbirth. In addition, the National Health Insurance program in Taiwan is a universal system of compulsory health insurance and has been implemented since March 1995. 29 It provides for 10 unpaid prenatal examinations during pregnancy. These programs avoid the previous incompleteness of birth registration and underregistration of infant death.
A significant portion of the mothers among intercultural couples immigrated to Taiwan for marriage and economic reasons. We had no detailed data for SES except for parental education level and residential distribution. Analyses of other information included public health intervention, although behavioral risk factors, such as smoking and alcohol consumption, were not available. The contributions of other possible sociodemographic disparities should also be considered in future studies. Although almost all the married immigrant mothers are Asian, their ethnicities could be further divided into different subgroups, such as Chinese, Vietnamese, Indonesian, and other Asian ethnic groups. Perinatal outcomes among Asians may vary by national origin. 30 Birth registration in our study was not linked to ethnic subgroups. Further subgrouping by national origin may provide important information.
In summary, evidence of a healthy immigrant mother effect on neonatal health is clear. Despite lower parental education, advancing paternal age, and spatial distribution disparity, babies born to married immigrant mothers in Taiwan had favorable neonatal outcomes. As global migration is changing the international landscape of healthcare needs, further research to explore unidentified risk or protective factors, such as economic status and physiologic or clinical condition, is important to improve perinatal outcomes among minority families. In addition, long-term follow-up studies are necessary to assess the extent to which observed intercultural differences will impact maternal and child health in the future.
Footnotes
Acknowledgments
The data used in this article were made available through the Taiwan birth and death registration databases. This study was supported by grants DOH89-TD-1040, DOH91-TD-1030, BHP-PHRC-92-4, and DOH93-HP-1702 from the Bureau of Health Promotion, Department of Health, Taiwan.
Disclosure Statement
The authors have no conflicts of interest to report.
