1. Introduction
Lower birthweights are associated with higher risks for cardiovascular and respiratory disease, diabetes, obesity, and premature mortality [
1,
2,
3,
4,
5]. Recently, there has been growing interest in how maternal exposure to nature may affect birthweight [
6,
7,
8,
9,
10,
11,
12,
13]. Prior studies found that increased maternal exposure to residential greenness, or natural vegetation around the home, was positively associated with birthweight. Greenness around the maternal residence is thought to improve health through mitigating exposure to air pollution, noise, and extreme temperatures; restoring mental health; and promoting physical activity and social engagement [
14]. Vegetation may buffer and reduce exposure to air pollution, noise, and heat [
15,
16,
17,
18]. Contact with greenness may also relieve stress and mental fatigue [
19,
20]. Higher residential greenness may provide increased access to recreational space and is associated with healthy behaviors such as physical activity and social contact [
19,
21,
22,
23]. Through these pathways, higher residential greenness may improve maternal health during pregnancy, which, as a consequence, may lead to a healthy fetal environment.
There remain gaps in understanding the relationship between residential greenness and birthweight. Although most prior studies showed positive associations between greenness and higher birthweights [
24], a few found null or negative associations [
6,
9]. The results from one recent study showed a positive association in Portland, Oregon, but a negative association in Austin, Texas, suggesting that there may be regional variation in how greenness is related to birthweights, perhaps due to differences in vegetation species type [
9]. Thus, it is important to investigate these associations in additional study settings. Furthermore, prior studies found that associations may differ depending on the maternal socioeconomic status (SES) or the SES of the neighborhood of maternal residence [
24]. Researchers have also found different associations depending on the population density near the residence [
7,
25]. We therefore, investigated the relationship between residential greenness and birthweight for all births in Massachusetts from 2001 to 2013. To further the understanding of this relationship, we assessed possible nonlinear associations by using natural splines. Moreover, as individual and neighborhood SES, as well as population density, may impact how mothers interact with residential greenness, we considered effect modification by SES indicators such as maternal education, government support for prenatal care, and Census median household income, as well as population density [
24,
26].
4. Discussion
In our analysis of Massachusetts singleton full-term live births from 2001 to 2013, we found a positive nonlinear association between maternal exposure to residential greenness during pregnancy and continuous birthweight. We observed stronger associations in the lower range of greenness (0.25–0.50 NDVI) than the higher range of greenness (0.50–0.75 NDVI) (
Figure 1). We observed linear inverse associations between greenness and the odds of TLBW or SGA. The association between greenness and TLBW or SGA was modified by SES indicators. For TLBW, the strongest associations were observed among those born to mothers with higher educational attainment. Associations did not change substantially when PM
2.5 was excluded from analyses, suggesting that the relationship between greenness and birthweight outcomes were not mediated by PM
2.5. Maternal education, government assistance for prenatal care, and Census block group median annual household income modified the relationship between greenness and SGA, with the strongest findings generally among mothers with higher SES. Stratified analyses also demonstrated somewhat stronger associations between greenness and TLBW among those living in high population density areas.
Several mechanisms could explain the association between greenness and higher birthweights. The main pathways are mitigating harmful environmental exposures, restoring mental capacity, and providing a setting for social interactions as well as physical activity [
14,
19,
26]. Vegetation such as trees may filter the air and serve as physical barriers to heat, air pollution, and noise [
24,
26]. Traffic air pollution has been shown to be considerably lower in areas of high greenness [
38]. Multiple studies have found that cognitive function and mental capacity improve with increased greenness exposure [
14,
19]. Moreover, since greenness often occurs in recreational spaces such as parks, high greenness is often indicative of proximity to places where people can meet socially or exercise, improving health through social cohesion and physical activity. Finally, although research directly looking at physiological responses to greenness is scarce, experiments have shown that proximity to greenness is associated with greater autonomic activity via measurements of heart rate variability [
39]. Other physiological findings include less pronounced response to stress and better immune function [
40]. Although the exact mechanism remains unclear, living in areas of higher greenness during pregnancy can result in unperturbed fetal growth through improved fetal oxygenation [
41]. Fetal hypoxia is a known cause of intrauterine growth restriction and mothers and increased greenness can potentially decrease this by improving overall maternal health through afore-mentioned mechanisms such as increased physical activity or decreased exposure to environmental stressors such as heat and noise [
14,
41]. In summary, conditions for a healthy fetal environment such as sufficient fetal perfusion and oxygenation are more likely to be met in mothers living in areas of higher greenness [
41], ultimately resulting in unperturbed fetal growth and increased birthweight [
10,
14,
24].
The majority of previous studies also found a positive association between greenness and continuous birthweight [
24], although our results fall in the lower range of existing estimates. Large positive associations were found in British Columbia, where a 0.1 NDVI increase was associated with a 20.6 (95% CI: 16.5, 24.7) g increase in birthweight [
13]; in a study in Tel Aviv, Israel, where a 0.06 NDVI increase was associated with a 19.2 (95% CI: 13.3, 25.1) g increase in birthweight [
42]; and in a pooled analysis of four Spanish birth cohorts a 38.3 (95% CI: 17.1, 59.5) g per 0.19 NDVI increase [
10]. It is possible that due to our conservative adjustment for different covariates, such as population density and air pollution, our estimates may be different from other analyses; however, we found that the associations between greenness and birthweight outcomes were similar when omitting PM
2.5 as a covariate (
Table A1). We found a positive nonlinear relationship between greenness and continuous birthweight (
Figure 1). In the lower range of greenness between 0.25 and 0.50 NDVI, the association was strongly positive. In the higher range of greenness between 0.50 and 0.75 NDVI, the association was positive but about half in magnitude. The characterization of a nonlinear dose-response relationship between greenness and continuous birthweight has not been previously reported unlike nonlinearity for other outcomes such as physical activity [
43]. In some prior studies of greenness and birthweight, it was not possible to determine the shape of the dose-response relationship since greenness exposure was classified into quantiles of NDVI [
8,
24]. Of some studies that considered NDVI on the continuous scale, one study used quadratic and cubic splines in their analysis, but did not find a departure from linearity [
7]. It is possible that the pathways through which greenness impacts birthweight in the lower range of greenness are different from those in the higher range of greenness. This may explain why positive, null, or even negative associations were found in existing literature [
24]. A recent study of over three million birth records in Texas found only a 1.9 (95% CI: 0.1, 3.7) g increase in birthweight when comparing those in the highest quartile of greenness (NDVI > 0.52) versus those in the lowest quartile (NDVI < 0.37) [
8]. Another study by Cusack et al. found a positive association for those born in Portland, Oregon, but a negative association for those born in Austin, Texas [
9]. Some studies did not find statistically significant changes in birthweight with increased greenness or proximity to green spaces [
6,
44].
Importantly, nonlinearity between greenness and health has policy implications. When considering potential benefits to birthweight by increasing greenness, it may be more beneficial to focus on developing climate-appropriate areas from low greenness to medium greenness, as opposed to developing from medium greenness to high greenness. However, as this is a novel finding, further investigation of the dose-response relationship between greenness and birthweight is needed.
Overall, higher greenness was associated with lower odds of TLBW and SGA. This was expected since there was a positive association between greenness and continuous birthweight. The association between increased greenness and lower odds of TLBW and SGA has previously been reported [
7,
12,
13,
24,
42]. With TLBW and SGA, we found the association with greenness to be linear and modified by population density (TLBW), maternal highest education attainment (TLBW, SGA), government support for prenatal care (SGA), and Census block group median household income (SGA). For population density, we found associations among those who reported living in high population density areas but not among those who reported living in low population density areas. A similar finding was published by Casey et al., who reported strong associations in cities but not in boroughs and townships (lower population density than cities) [
7]. In a separate analysis, the association between greenness and depressive symptoms in adolescents was also reported to be stronger among those in high population density areas but not in low population density areas [
25]. The mechanisms behind why population density modifies associations with greenness are unclear, but it was possible that greenness helped decrease detriments from exposures that were present in high population density areas but not in low population density areas [
24,
26]. Those with higher education attainment or without government support for prenatal care had higher individual SES [
45,
46]; higher Census block group median household income was also indicative of higher neighborhood SES. Our results stratified by SES did not demonstrate a monotonic relationship; however, they were suggestive of stronger associations among those born to mothers of higher individual or neighborhood SES. This finding contrasts those previously reported in the literature [
14,
24], which concluded that greenness associations were stronger among those with lower SES. Individual and neighborhood SES can alter how one interacts with greenness, such as accessing nearby areas of greenness. It was possible that lower individual or neighborhood SES hinders true access to areas of greenness, thus leading to weaker associations [
14]. Those with lower individual SES might not be as likely to access areas of surrounding greenness or there might be safety concerns in areas of lower neighborhood SES discouraging access of green areas. In summary, the overall associations between greenness and lower odds of TLBW and SGA was consistent with previous studies. However, patterns in how SES indicators modified these associations contrast most previous findings, demonstrating that how SES impacts potential health effects of greenness is variable, complex, and warrants further investigation.
Our study had strengths and limitations. With a final sample size of 780,435, which represents one of the largest studies on the relationship between greenness and birthweight to date [
8,
24], the study had high statistical power and the ability to assess nonlinear associations as well as effect modification by SES indicators. For greenness exposure assignment, we used multiple temporally-matched measurements to determine exposure during pregnancy. Therefore, we captured the time-varying nature of greenness which is likely more accurate than prior studies that used only a single satellite image from, for instance, one summer day [
6,
12,
44]. This likely reduced bias from exposure misclassification. That said, exposure assignment was limited by basing all calculations on maternal residence reported at the time of birth, and mothers may have changed addresses since conception. We could not check if there were errors in maternal residence or other included model covariates, but we expect the bias from such measurement error to be non-differential. Furthermore, some births in the complete database had to be excluded because of missing maternal residence information. But since there was relatively low exclusion due to missing maternal residence, bias from this source was likely minimal. Another limitation with greenness exposure was our choice to use NDVI. Although it is an established measure of greenness [
27], it does not provide information on the specific types of vegetation such as trees, grass, or shrubs, nor does it describe accessibility of green spaces. How mothers interacted with greenness depending on the type of vegetation could be very different and without this information, we were unable to devise specific recommendations on types of vegetation that might be most associated with higher birthweights and lower odds of TLBW or SGA [
14,
24,
26]. In fact, the variety of estimated associations for greenness in the existing literature could be due to differences in vegetation species types across study settings. By using 250 m as the spatial resolution, we assumed that pathways through which greenness influences fetal growth were limited the mothers’ activity in the immediate area around their residence. While prior studies found no considerable differences in associations when using 100, 250, 500 and 1250 m spatial resolutions [
6,
7,
42], it is unclear that only local residential greenness influenced fetal growth. Finally, the generalizability of some of our findings was limited due to the demographics of the study population. Almost three-quarters of the mothers were white and over three-quarters reported living in high population density areas. Our finding of stronger associations among those with higher SES, which was inconsistent with most existing literature on greenness and birth outcomes [
24], could be explained by differences in demographics between study populations.