Objective
We sought to investigate seasonal variation in fetal growth, accounting for important sociodemographic, biological, and environmental exposures.
Study Design
Records of births 1998 through 2006 in Perth, Western Australia were obtained (N = 147,357). We investigated small for gestational age and sex and the proportion of optimal birthweight (POBW) in relation to seasonal exposures (season, temperature, sunlight) by trimester of pregnancy. Adjustment was made for a wide range of risk factors.
Results
The POBW for neonates with third trimesters predominantly in summer was 0.18% (0.00-0.36%) lower than for those in winter. POBW decreased by 0.14% (0.01-0.27%) per interquartile range increase in third-trimester temperature (9.15°C). An interquartile range increase in temperature over pregnancy (0.73°C) was associated with an odds ratio of 1.02 (95% confidence interval, 1.00–1.05) for small for gestational age and sex.
Conclusion
Reduced fetal growth was associated with elevated ambient temperatures throughout and late in pregnancy, independently of air pollution and other risk factors.
Birthweight is highly indicative of infant mortality and morbidity, and may play a role in adverse health outcomes later in life. As a full range of anthropometric measurements during the intrauterine period is rarely available on a population basis, birthweight is typically used to retrospectively assess the appropriateness of fetal growth in a single metric. Fetal growth and subsequent birthweight is associated with a range of biological, socioeconomic, dietary, ethnic, and parental factors. Reduced birthweight has been observed with adverse environmental exposures and elevated maternal blood pressure causing vasoconstriction and reducing blood flow to the fetus. Birthweight may be affected by certain environmental exposures, including prenatal exposure to maternal smoking, lead, chemical agents (eg, pesticides), environmental tobacco smoke, outdoor air pollution, and drinking water contaminants. A number of predictive factors relevant to birthweight may also be modified by seasonality, including environmental/climatic variables (temperature, sunlight, exposure to ambient air pollutants ), maternal exposures/behaviors (nutritional intake, infection, physical activity, environmental tobacco smoke ), and biological processes (pregnancy-induced hypertension ). It is important to recognize the importance of the seasonal variation in fetal growth because some of the potential causes listed above may be modifiable. Moreover, in studies that estimate birthweight, failure to fully adjust for these factors may result in confounded results. For example, in the case of exposures to air pollution, cyclical fluctuations and photochemical reactions influence the levels of criteria air pollutants in the atmosphere and seasonal effects on fetal growth must be considered in studies.
Published reports of the observed annual pattern of seasonal variation in fetal growth are inconsistent. Various studies in developed countries have linked a wide range of seasonal factors to lower birthweights. Difference in latitude has been offered as an explanation for such discrepancy, and a vitamin D hypothesis followed as a consequence. However, latitude is closely related to climate and therefore may be a surrogate for weather conditions, such as temperature. This demonstrates the need to investigate temperature and sunlight exposure, which are more specific correlates of climate than latitude and can be attributed to a biologically plausible mechanism.
The objective of this study was to investigate fetal growth in relation to seasonal exposures and identify the vulnerable stages of pregnancy, after accounting for a range of important sociodemographic, biological, and environmental exposures.
Materials and Methods
Study population and setting
The study population included all singleton live births in metropolitan Perth, Western Australia, in the period from 1998 through 2006. Records were obtained from the Midwives Notification System, which contains birth notifications completed at the time of separation for every still born or live born baby of ≥400 g birthweight and/or ≥20 weeks’ gestation in Western Australia. The collection includes information on maternal demographic characteristics, maternal health, pregnancy, labor, delivery, and infant outcomes.
Perth is the capital of Western Australia and lies at 31 degrees latitude south of the equator. Being in the southern hemisphere, winter occurs in June through August and summer in December through February. The weather in Perth is very different to northern hemisphere weather patterns; summer and winter temperatures average around 30°C and 18°C, respectively. The population is geographically concentrated in the capital, Perth, with almost 75% of the state’s total population of approximately 2 million (2004) living in the metropolitan area.
Description of outcome and explanatory factors
The primary outcome was fetal growth: small for gestational age/sex (SGA) and the proportion of optimal birthweight (POBW). SGA was calculated based on the Australian national birthweight percentiles whereby infants with a weight for gestational age <10th centile for their sex were defined as SGA. POBW was calculated using the ratio of each individual observed birthweight to optimal birthweight and expressed as a percentage. POBW is unitless because it is a ratio of 2 weights. This model for optimal birthweight, developed by Blair et al, accounts for constitutional growth potential by controlling for gestational age, maternal height, birth order, and infant sex and was developed using an independent birth cohort free of known recorded risk factors. We investigated only births of at least 33 weeks of completed gestation because POBW is potentially less accurate before this time.
Seasonal and environmental data were obtained from the Australian Bureau of Meteorology and the Western Australian Department of Environment, respectively. Seasonal exposures were defined as daily maximum temperature (°C) and hours of sunlight and based on data from the Perth metropolitan area site (location no. 009225) and airport site (location no. 009021). Daily metropolitan levels of criteria air pollutants, including particulate matter with aerodynamic diameter <2.5 μm (PM 2.5 ) and <10 μm (PM 10 ), ozone, nitric oxide (NO), nitrogen dioxide (NO 2 ), and carbon monoxide (CO) were obtained from measurements taken at 10 metropolitan air pollutant monitoring stations. Environmental measurements were averaged across all 10 monitoring stations in the study region to obtain citywide pollutant levels. Averaging was applied because not all of these pollutants were monitored at every site, which made it inappropriate to use the nearest monitor approach that has been applied in other air pollution analyses. Daily levels of pollution, temperature, and sunlight were obtained for each day of pregnancy for each woman in the cohort and then averaged over the entire duration pregnancy and over each trimester of pregnancy separately.
As trimesters of pregnancy typically do not overlap exactly with climatic seasons, we used temperature to assist in a more appropriate definition of season of first, second, and third trimesters. The average temperature in third trimester was lowest for August through October births and highest for February through April births, so we defined births during these periods as having winter and summer third trimesters, respectively. This definition is intuitively more sensitive to early and late seasonal changes. Similarly, season of first trimester and second trimester were defined using weeks 13 and 26 of gestation.
Statistical analyses and adjustment
Descriptive statistics for maternal and infant characteristics and measurements of seasonal and criteria pollutants were calculated. The association of SGA and POBW was investigated in relation to seasonal exposures (season, temperature, sunlight) for each trimester of pregnancy and season using logistic and multiple linear regression, respectively, using SAS 9.1 software (SAS Institute Inc, Cary, NC). We presented results for interquartile range (IQR) (75th–25th percentile point) increases in temperature, sunlight, and air pollutants. The IQR represents the range of the middle 50% of exposures. Exposures were divided by the IQR to gauge the effect of an increase in exposure from typically low to typically high levels.
In multivariate models adjustment was made for maternal condition/complication (gestational and preexisting diabetes, preeclampsia, indigenous status, married/de facto relationship status, and smoking during pregnancy). We also adjusted for criteria air pollutants (PM 2.5 , PM 10 , ozone, NO, NO 2 , and CO) and socioeconomic status using the socioeconomic index for areas advantage-disadvantage score obtained from the Australian Bureau of Statistics. Due to the large number of comparisons, we conducted multivariate analyses only for criteria air pollutants and meteorological variables statistically significant at the 5% level in univariate analyses.
Assessment of multicollinearity
The presence of multicollinearity was assessed by calculating variance inflation factors (VIFs) for effect estimates obtained from both multiple and logistic regression models. The square root of the VIF is interpreted as the factor by which the SE is inflated compared to the situation in which the explanatory variables are completely uncorrelated.
Ethics approval
Approval for this study was granted by the University of Western Australia (project: RA/4/1/2006) and the Department of Health Western Australian Human Research Ethics Committee (project: 2008/7).
Results
Maternal and infant characteristics
There were 147,357 singleton live births in the metropolitan Perth area from 1998 through 2006 ( Table 1 ). The most prevalent groups in the study were women aged 30-34 years (33%), those having a first birth (43%), and women in a married or de facto relationship (91%). A total of 4100 women (3%) were of Aboriginal ethnicity and 24,442 women (17%) reportedly smoked during pregnancy. Approximately 5% of births were preterm. A total of 13,098 women (9%) experienced preeclampsia or had preexisting or gestational diabetes. The mean birthweight was 3409 (SD 499) g and a total of 12,031 births (8%) were classified as SGA.
| Maternal and infant characteristics | n (%) |
|---|---|
| All births | 147,357 |
| Maternal | |
| Age, y | |
| <20 | 6813 (5) |
| 20-24 | 21,727 (15) |
| 25-29 | 41,863 (28) |
| 30-34 | 49,001 (33) |
| ≥35 | 27,953 (19) |
| Parity | |
| First birth | 62,713 (43) |
| Second birth | 50,308 (34) |
| Third birth | 21,919 (15) |
| ≥Fourth birth | 12,417 (8) |
| Aboriginal or TSI | 4100 (3) |
| Married or de facto | 134,141 (91) |
| Medical condition/pregnancy complication a | 13,098 (9) |
| Smoked during pregnancy | 24,442 (17) |
| SEIFA index, mean (SD) | 1015 (87) |
| Infant, n (%) | |
| Male | 75,221 (51) |
| Female | 72,134 (49) |
| Preterm birth (<37 wk) | 7479 (5) |
| SGA | 12,031 (8) |
| POBW (%) mean (SD) | 99 (12) |
| Birthweight, g | 3409 (499) |
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