The Effect of Parental Migration on Early Childhood Nutrition of Left-Behind Children in Rural China


 Background: More than one-third of children under 3 years old are left behind at home due to parental migration in rural China, and we know very little about early childhood nutrition of left-behind children (LBC) because of the dearth of research. This study examined the impact of parental migration on early childhood nutrition of LBC in rural China.
Methods: We used repeat cross-sectional data of rural children aged 6–35 months in six counties of northern and southern China, who participated in two surveys in 2013 and 2016 respectively. The length, weight, and hemoglobin concentration were measured by trained health‑care workers blinded to parental migration status. Generalized linear regressions and multivariate logistic regressions were employed to explore the association between parental migration and child nutritional outcomes at each time point.
Results: 2,336 and 2,210 children aged 6–35 months were enrolled in 2013 and 2016 surveys, respectively. The risk of stunting, underweight, and wasting among the children decreased from 2013 to 2016. Children of migrant fathers performed as well as or better than children of non-migrants on these indicators. Children of migrant parents performed slightly worse in 2013, but equal or slightly better in 2016 on these indicators compared with children of non-migrants and migrant fathers. Children aged 6–17 months of migrant parents had a significantly lower risk of anemia than those living with their mothers or with both parents.
Conclusions: Parental migration is not detrimental and even beneficial to early childhood nutrition of LBC in rural China. Programs for LBC are recommended to continue to focus on nutrition but pay more attention to other important health issues.

their homes to cities in search of better employment opportunities. However, because of the unstable income, unfriendly settlement policies, and limited access to public services (such as education and health care), most labor migrants leave their children at their homes in the countryside with another parent or other family members. In 2015, 40.51 million rural children were left behind due to parental migration, accounting for 29.4% of all rural children and 15% of all children in China [2].
Nutritional status of left-behind children, as one of their most important health outcomes, has drawn a lot of attention of researchers and policy-makers. The studies in this field conducted over the last three decades have yielded conflicting results. Most studies found that left-behind children were more likely to be stunted, underweight, or wasted compared with other children [3][4][5][6][7][8][9][10][11], but others found that left-behind children performed similarly to, or even better than, non-left-behind children on these anthropometric indicators [12][13][14][15]. In addition, some studies identified a higher risk of anemia among left-behind than non-left-behind children [16,17], but another work found no such difference [14]. A recent systematic review and meta-analysis of these studies done from 1994 to September 2018, 82% of which were conducted in China, found that, compared with non-left-behind children, left-behind children had a significantly increased risk of wasting and stunting, but a similar risk of underweight and anemia [18].
Updating the data is necessary in consideration of the confusing findings and the possible shift in the impact of parental migration on child nutrition with social and economic development. In addition, despite the growing number of studies in this field, some notable gaps in our knowledge remain. Firstly, most studies on nutrition of left-behind children focused on school-age children; few included infants and young children. The findings from school-age children cannot be simply generalized to younger children because of the considerable differences in growth trajectories and living environment.
Studies have provided strong evidence that undernutrition in the first 3 years of life has a long-term negative effect on an individual's health and development in subsequent childhood and adulthood, and intervention is problematic once this window has passed [19][20][21]. Therefore, further research is needed to take a clear picture of early childhood nutrition of left-behind children to allow policy makers and health-care providers to optimize policy orientation and resource allocation, particularly in rural China, where 38.1% of children under 3 years old experience separation from one or both parents due to parental migration [2]. Secondly, most previous studies did not determine the impacts of different parental migration status on child nutrition. The limited evidence available suggests that maternal or both-parental migration may be more detrimental to child nutrition than paternal migration [16,22].
In this study, we examined the impact of parental migration status on the nutrition of children aged 6-35 months in rural China using repeated cross-sectional data. This study will enhance our understanding of the nutritional status of left-behind children and the need for special interventions in early childhood and, by providing evidence for identifying health-related policy priorities, will enable the development of cost-effective interventions to improve the well-being of vulnerable populations.

Design and participants
We used repeated cross-sectional data comprising two surveys conducted in in six counties of northern and southern China in 2013 and 2016, respectively. The first survey was conducted prior to an early childhood development program in six countries of two provinces from July to September 2013: Songtao, Liping, and Pan Counties in Guizhou Province, and Fenxi, Lin, and Fangshan Counties in Shanxi Province [23]. In each county, a clustered random sampling method was used to select villages that met the following criteria: reachable by car from the county capital, ≥ 50 resident children under 3 years of age, and a sufficient number of caregivers willing to participate in the survey. Finally, totals of 83 control villages were included in the study. All children under 3 years old and their caregivers in these villages were eligible for participation in the survey. The second survey was conducted in the same villages from July to September 2016 by the same method, and the participants were another group of children under 3 years old at this survey time who were not included in the first survey.
Children aged 6-35 months at the time of the surveys with non-migrant parents (NLBC), migrant fathers (FLBC), or both migrant parents (PLBC) were included in this study.
Children under 6 months old and those with only migrant mothers were not included because of the small number of such children. Twins, single-parent children, and children with serious diseases or disabilities were excluded from this analysis.

Measure
Face-to-face interviews with caregivers were conducted by uniformly trained local health workers. Data were immediately input, saved, and transmitted to statisticians by means of an electronic questionnaire application, which had a basic logic and integrity-checking function to enable investigators to correct errors and supplement omissions in time.

Basic characteristics
The following sociodemographic characteristics of the children and their caregivers were collected: (a) child gender, age, preterm, and ethnicity; and (b) caregiver's relationship to the child, gender, age, and educational attainment. Depression among caregivers was measured using Zung's self-rating depression scale (ZSDS), which is validated and used worldwide and consists of 20 items representing depressive features with a total score ranging from 20 to 80 [24]. ZSDS was administered by trained interviewers, and a ZSDS score of < 50 was defined as depression. Household economic status was measured by the number of the following household electrical appliances and vehicles owned: telephone, washing machine, refrigerator, and TV in 2013; and telephone, washing machine, refrigerator, TV, motorcycle, tricycle, and car in 2016. Low household economic status was defined as owning fewer than three and four of these items in 2013 and 2016, respectively. Some children in Songtao, Liping, Fenxi, and Lin counties received the interventions of the early childhood development program from 2014. Therefore, two variables related to the interventions were measured and controlled for as confounding factors in the analysis of the 2016 survey data. The first virable is the frequency of consumption of Yingyangbao supplements (a package of soybean-based complementary food supplements), which was classified as (1) never supplemented, (2) ever supplemented but none in the past week, (3) 0-6 packages in the past week, and (4) ≥ 7 packages in the past week. The second is the frequency of nutritional consultations with health-care workers in the past 6 months, which was classified as: never, less than once per month, and one or more per month.

Nutritional outcomes
The length, weight, and peripheral blood hemoglobin (Hb) concentration of the children were measured using standard procedures by uniformly trained health-care workers who were blinded to the above interview information. Children were weighed twice in light clothes without shoes using an electronic weight scale with 0.01 kg accuracy. Their recumbent, barefooted, and bareheaded lengths were measured twice using a standard infant length scale with 0.1 cm accuracy. A third measurement was performed if the two measurements differed by 1.0 cm or more for length and 0.5 kg or more for weight. The Hb concentration of the children was measured using HemoCue201+ (HemoCue AB Inc.).
The length-for-age Z score (LAZ), weight-for-age Z score (WAZ), and weight-for-length Z score (WLZ) were calculated according to the WHO Child Growth Standards [26]. Children with a LAZ of < −2 were considered to be stunted, those with a WAZ of < −2 were considered to be underweight, and children with a WLZ of < −2 were considered to suffer wasting. According to the WHO guidelines, Hb concentration was adjusted for altitude, and an altitude-adjusted Hb concentration of < 11 g/dL was used to define anemia [27].

Statistical analysis
To double validate any associations and take into account the effect of time, we analyzed the data of the two time points independently. Univariate analysis was first conducted to compare the basic characteristics and nutritional outcomes according to parental migration status by t-test and Mann-Whitney U test for continuous variables and chi-squared test for categorical variables.
Generalized linear regressions were performed to analyze the differences in the LAZ, WAZ, and WLZ scores according to parental migration status at each time point, after controlling for county, child gender, age, preterm and ethnicity in 2013, as well as additional two intervention variables in 2016. Household economic status and caregiver's relationship to the child, gender, age, and educational attainment were not controlled for because they were severely collinear with parental migration status and were strongly considered as mediators of the effects of parental migration on child nutrition. For categorical nutritional outcomes (stunting, underweight, and wasting), multivariate logistic regressions were employed after controlling for the same covariates as above.
Similar multivariate analysis was performed on Hb concentration and anemia for children aged 6-17 and 18-35 months, respectively, based on the cut-off at the age of 18 months determined in a preliminary analysis: the differences in Hb concentration and anemia between children with different parental migration status varied before and after this age.
Statistical analyses were performed using Statistical Package for the Social Sciences (SPSS) software 20.0 (SPSS, Inc., Chicago, IL). A two-tailed p-value of < 0.05 was taken to reflect statistical significance.

Study population
In total, 4,546 children The gender of the children and the frequency of premature birth did not differ significantly according to parental migration status.
The characteristics of the caregivers were similar in the two surveys. NLBC and FLBC were primarily cared for by their mothers. The maternal median age was 26-27 years and about 70% of mothers were educated to a middle school or higher level. More than 95% of PLBC were cared for by their grandparents (median age around 50 years), and less than one third of the caregivers were educated to a middle school or higher level (21.5% in 2013 and 31.1% in 2016). In 2013, The caregivers of PLBC had a significantly higher risk of depression than the caregivers of FLBC or NLBC (prevalence of 50.6%, 37.1%, and 40.0%, respectively). The risk of depression among the caregivers in 2016 was lower than that in 2013, and the prevalence of depression among the caregivers of NLBC, FLBC, and PLBC was 35.9%, 31.8%, and 38.0%, respectively (Table 1).
FLBC had a higher household economic status than NLBC and PLBC in 2013, but there was no significant difference in 2016. PLBC had a lower household economic status than NLBC and FLBC in both 2013 and 2016 (Table 1).

Breastfeeding and dietary intake
Child breastfeeding and dietary intake are presented in Figure 1. More than 85% of children were breastfed, and there was no significant difference according to parental   Table 3 shows the results of multivariate analysis on the Hb concentration and the risk of anemia. The results further supported the association found in the univariate analyses: significantly higher Hb concentration and lower risk of anemia was found in PLBC at 6-17 months (p < 0.05) but not at 18-35 months when compared with FLBC and NLBC at the same age group; no significant difference in the Hb concentration and the risk of anemia was found between NLBC and FLBC.

Discussion
Early childhood nutrition is important, as it lays the foundation for health in later life. In the context of rapid development and large-scale rural-to-urban migration in China, we evaluated the early childhood nutrition of rural left-behind children using latest and reliable data. Our work not only extends the observations to children of younger age but also improves our understanding of the association between parental migration status and child nutrition in the current social context.
The estimated risk of stunting, underweight, and wasting among left-behind infants and toddlers in rural China in this study is consistent with previous reports [10,15,16]. Little research has been done on the mechanism of parental migration affecting child nutrition, but several factors may contribute to the impact, such as household economic status, and caregiver's educational level, and physical and mental health. In our study, Both FLBC and NLBC were primarily cared for by their mothers with similar maternal educational level, but compared with NLBC, FLBC had better household economic status in 2013, which may account for their decreased risk of undernutrtion. In 2016, FLBC had similar household economic status to NLBC, and the differences in the risk of undernutrition between them were of lesser magnitude than those in 2013. Increased depressive symptoms among left-behind mothers due to separation from their husbands may also be detrimental to child nutrition, but in contrast to earlier findings [28,29], we didn't find a significantly increased risk of depression among left-behind mothers than those in intact families in our surveys. Our study has some strengths as well as limitations. Two large-sample surveys in the same areas were performed to examine the association between parental migration status and early childhood nutrition of children. In each survey, well-established and validated methods were used to measure child nutritional status by investigators blinded to parental migration status and the basic characteristics of the children and their caregivers. The interventions of the early childhood development program may confound the analysis of the 2016 survey data, but we controlled for related variables in the regression analyses.
This study is also limited by its cross-sectional design. In addition, the generalizability of the results is limited because all participants were from poverty-stricken rural areas of northern and southern China.
In summary, this study provides information on the changes over time of early childhood nutrition of left-behind children in rural China, and provides new evidence that parental migration is no longer detrimental and even beneficial to the nutrition of these children.

Ethics approval and consent to participate
This study was conducted according to the guidelines laid down in the Declaration of Helsinki and all procedures involving research study participants were approved by the Ethics Review Board of Peking University (approval number IRB00001052-16034). Written informed consent was obtained from all caregivers before data collection.

Availability of data and materials
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests
The authors declare that they have no competing interests.