JRMS J Res Med Sci Journal of Research in Medical Sciences Journal of Research in Medical Sciences 1735-1995 1735-7136 Medknow Publications Pvt Ltd India JRMS-18-875 24497859 Original Article Association between air pollution and preterm birth among neonates born in Isfahan, Iran Janghorbani Mohsen Piraei Janghorbani Department of Epidemiology and Biostatistics, Isfahan University of Medical Sciences, Isfahan, IranDepartment of Epidemiology and Biostatistics, Isfahan University of Medical Sciences, Isfahan, Iran Address for correspondence:Mohsen Janghorbani, Department of Epidemiology and Biostatistics, School of Public Health, Isfahan University of Medical Sciences, Isfahan, Iran janghorbani@hlth.mui.ac.ir October 2013 18 10 875 881 1252013 2652013 Copyright: © Journal of Research in Medical Sciences 2013

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Background:

Although several studies have investigated the association between maternal exposure to air pollution and preterm birth, the results are inconsistent. The aim of this study was to further investigate the relation between maternal exposure to ambient air pollution during pregnancy and the risk of preterm birth and low birth weight (LBW) in an Iranian pregnant population. Materials and Methods:

In this study, we identified 4758 consecutive singleton birth records from one large referral hospital (2010-2012) in Isfahan, Iran. We identified cases of preterm birth and LBW, which were combined with meteorological and air pollution monitoring data. We estimated the effect of air pollution exposure during the entire pregnancy, each trimester, and last month, and preterm birth (gestational age <37 weeks) and LBW (<2500 g) by Pollutant Standard Index (PSI) using logistic regression adjusted for gestational age, neonate gender, birth order, and mother′s age. Results:

The PSI for entire pregnancy was significantly associated with preterm birth [Odds Ratio (95% CI) = 1.26 (1.20, 1.33)]. There was no association between maternal exposure to ambient air pollution and each trimester and the last month of pregnancy, and preterm birth or LBW. Conclusion:

Maternal exposure to ambient air pollution during the entire pregnancy was associated with preterm birth in Isfahani women.

Materials and Methods:

In this study, we identified 4758 consecutive singleton birth records from one large referral hospital (2010-2012) in Isfahan, Iran. We identified cases of preterm birth and LBW, which were combined with meteorological and air pollution monitoring data. We estimated the effect of air pollution exposure during the entire pregnancy, each trimester, and last month, and preterm birth (gestational age <37 weeks) and LBW (<2500 g) by Pollutant Standard Index (PSI) using logistic regression adjusted for gestational age, neonate gender, birth order, and mother′s age. Results:

The PSI for entire pregnancy was significantly associated with preterm birth [Odds Ratio (95% CI) = 1.26 (1.20, 1.33)]. There was no association between maternal exposure to ambient air pollution and each trimester and the last month of pregnancy, and preterm birth or LBW. Conclusion:

Maternal exposure to ambient air pollution during the entire pregnancy was associated with preterm birth in Isfahani women.

Results:

The PSI for entire pregnancy was significantly associated with preterm birth [Odds Ratio (95% CI) = 1.26 (1.20, 1.33)]. There was no association between maternal exposure to ambient air pollution and each trimester and the last month of pregnancy, and preterm birth or LBW. Conclusion:

Maternal exposure to ambient air pollution during the entire pregnancy was associated with preterm birth in Isfahani women.

Conclusion:

Maternal exposure to ambient air pollution during the entire pregnancy was associated with preterm birth in Isfahani women.

Air pollution low birth weight Pollutant Standard Index pregnancy outcome premature birth preterm delivery
</sec><sec><title>Introduction

Preterm birth (before 37 gestational weeks) and low birth weight (LBW) are leading causes of neonatal morbidity and mortality as well as possible increased morbidity in adulthood, 1,2 and its rate is increasing worldwide, 3 affecting 13-15% of births. 4 Families of preterm neonates also bear a substantial economic burden, including inpatient hospital costs 5,6 and long-term health care costs during the first year 6,7 and through early childhood. 7,8,9 The etiology of the majority of preterm births remains unknown. Thus, it is necessary to identify the risk factors for preterm delivery and work toward their prevention. Although over the last two decades or so, several studies mainly performed in North America and Australia have investigated the possible adverse effects of exposure to ambient air pollution during different periods of pregnancy on preterm birth/LBW, the role of air pollution as a risk factor for preterm birth/LBW is small and not always consistent. 10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27 In most studies, the risk of preterm delivery was slightly increased, 12,13,14,15,19,20,21,24 whereas others reported no association. 11,16,22,23,25,26,27,28 The risk of preterm delivery was stronger than LBW 19 or the opposite was observed 20 or inconclusive results were obtained, 17,18 making the results of these studies difficult to interpret. The inconsistency noted between studies may be related to many factors, including chance, sample size, design, risk factors, and variation across the population, differing analytic methods, and issues related to data quality and measurement error and other characteristics.

While there have been abundant epidemiological studies in Western countries, no study has been undertaken in Iranian pregnant women, where the ambient air pollution patterns and ethnicity are different. However, from clinical and public health point of view, it is important to clarify the role of ambient air pollution in association with preterm birth/LBW because the growing fetus may be particularly susceptible to the toxic effects of air pollution. Our study contributes to this issue by examining the association between ambient air pollution, measured by Pollutant Standard Index (PSI) during entire pregnancy, 1 st , 2 nd , 3 rd trimesters, and the last month of pregnancy, and preterm birth/LBW in Isfahan, Iran. Our hypothesis is that exposure to air pollution contributes to the etiology of preterm birth/LBW.

Materials and Methods

Study area

This study was conducted in Isfahan, a very large area where the pollutant levels are high. This place is situated in central Iran, located at a height of 1590 m above the sea level, between latitudes 30° and 34° north of the equator and longitude 49°-55° east, with a population of approximately 1.8 million (1,799,180 in 2004 (men 926,134, women 873,046)). The total area is 15,263 km 2 . The climate is dry and temperate, with quite wide temperature differences between the summer and the winter with a mean daily temperature of 2.8°C in January and February, 29.5°C in July and August, and 19.1°C in September and October. The mean annual precipitation is 146.0 mm (reference period 2004). Major pollutant sources include vehicles and stationary combustion sources.

Subjects

The birth records of 4758 healthy pregnant women without major structural birth defects were identified from Beheshti Obstetrics and Gynecology Hospital (largest women′s hospital in Isfahan) affiliated to the Isfahan University of Medical Sciences, Iran between January 2010 and June 2012. Pregnant women were eligible if they were living in those urban areas of Isfahan city with air pollution monitoring stations. Entry criteria included healthy pregnant women of 18-35 years, with no complicated pregnancy, carrying a singleton fetus, and living in Isfahan. Tenets of current version of the Declaration of Helsinki were followed; study protocol was reviewed and approved by the institutional ethical committee of Isfahan University of Medical Sciences.

Definitions

Preterm birth was the main outcome evaluated, which was defined as a singleton live-birth delivery before 37 completed weeks of gestation. Gestational age was computed on the basis of the date of a woman′s last menstrual period (LMP) supported by an ultrasound scan. For women whose LMP date was missing, the clinical estimate of gestational age was substituted. No individual information is available about whether or not the gestational age was based on an ultrasound examination or the date of the LMP. We used the estimate of gestation in completed weeks to back-calculate the date of conception. LBW was defined as weight at birth less than 2500 g.

Air pollution data

Data of the four existing fixed-site air-monitoring stations in the Isfahan city were used to represent the exposure of participants to air pollutants. For categorizing the air quality measurement, we used the PSI for five major pollutants routinely monitored in many parts of the world [CO, O 3 , NO 2 , SO 2 , and particulate matter less than 10 μm (PM 10 )]. The PSI converts air pollution concentrations to a simple number between zero and 500 and assigns descriptive terms such as "good" or "moderate" to that value. PSI values of 0-50 and 51-100 indicate good and moderate air quality, respectively. A PSI value of 100 indicates that at least one pollutant reached its ambient air quality standard on that day. PSI values of 101-150 show that the air quality is unhealthy for sensitive groups, and values of 151-200 indicate unhealthy air. A PSI of 200 corresponds to a first-stage alert during which time elderly persons with existing heart or lung disease are advised to stay indoors and reduce their physical activity; and PSI values of 201-300 indicate very unhealthy air. A second-stage alert is called when the PSI reaches 300, at which point the general public is advised to avoid outdoor activity, i.e., PSI values of 301-500 indicate hazardous air quality. Pollution data on the entire pregnancy period, at the 1 st (defined as gestational weeks 1-13), 2 nd (defined as gestational weeks 14-26), and 3 rd (defined as from 27 weeks to birth) trimesters, and at the last 4, 6, and 8 weeks before birth day and at birth day were collected and the citywide daily average levels was matched for each woman. PSI data were matched with the time of pregnancy for each woman to estimate pollution effects on preterm/LBW. To estimate pollution effects on preterm/LBW, we calculated for every participant, the average PSI concentration during the entire pregnancy, at the 1 st , 2 nd , 3 rd trimesters, and at the last month and last week of pregnancy from the daily average concentration.

Statistical analysis

Statistical methods used included the Student′s t-test, one-way analysis of variance (ANOVA), chi-squared test, and binary logistic regression. Comparisons between quartile of PSI were calculated by ANOVA followed by Tukey-Kramer post-hoc comparison. Univariate and multivariate binary logistic regressions were fitted to identify predictors of preterm birth/LBW using the SPSS version 18 for Windows (SPSS Inc., Chicago, IL, USA). Two models were used to assess the relationship between PSI for the entire pregnancy, the 1 st , 2 nd , and 3 rd trimesters, and the last 4, 6, and 8 weeks before birth day and at birth day, and preterm birth/LBW; the first model was unadjusted and the second model was adjusted for maternal age, neonatal gender, and birth order. Age-adjusted means were calculated and compared using general linear models. All tests for statistical significance were two-tailed and performed assuming a type I error probability of <0.05.

Results

Characteristics of the 1069 (22.5%) neonates with preterm birth and 3689 (77.5%) neonates with term birth, as well as of 837 (17.6%) neonates with birth weight <2500 g and 3921 (82.4%) neonates with birth weight ≥2500 g are shown in Table 1. Women with preterm birth/LBW were older and had lower maternal age-adjusted mean gestational age and PSI for 2 nd and 3 rd trimesters, and those with LBW had lower proportion of boys and higher proportion of 1 st birth order. The gender of the neonate was not associated with preterm birth. The mean (SD) maternal age was 27.7 (7.0) years for those with preterm birth and 26.9 (6.5) years for those with term birth. The mean (SD) PSI for the entire pregnancy was 103.4 (3.2) for those with preterm birth and 103.2 (4.1) for those with term birth. The total PSI for the entire pregnancy ranged from 85.6 to 128.3.{Table 1}

The characteristics of the study participants by PSI for the entire pregnancy quartile are shown in Table 2. In age-adjusted comparisons of variables, all PSI variables were more likely to slightly increase and gestational age was more likely to slightly decrease across the four subject groups. {Table 2}

To determine the independent predictors of factors associated with preterm birth/LBW, stepwise binary logistic regression was used to test 12 predictor variables [mother′s age, birth order, infant gender (male and female), PSI for the entire pregnancy, 1 st , 2 nd , and 3 rd trimesters, and the last 1, 4, 6, and 8 weeks before birth day and at birth day]. The dependent variable was birth under 37 weeks of gestation or birth weight <2500 g.

In crude and adjusted analyses, there was a significant positive association between PSI levels and preterm birth during the entire pregnancy [Odds Ratio (OR) (95% CI) = 1.26 (1.20, 1.33)]. No association was found between PSI and preterm birth/LBW in all exposure periods. Controlling for mother′s age, neonate′s gender and birth order did not appreciably alter the OR compared to the unadjusted model Table 3. There was no indication for an adverse effect of air pollution on LBW from these analyses. {Table 3}

Discussion

We studied the association between ambient air pollution, measured by PSI during entire pregnancy and eight gestational windows, and preterm birth/LBW in Isfahan, Iran. Our analysis suggests that ambient air pollution during the entire pregnancy may have an impact on preterm birth, but not on LBW. There was no association between air pollution at particular gestational windows and preterm birth/LBW. There could be several explanations to these null effects. One possible explanation is that there is no effect. The other possible explanation for these null results could be an underestimation of effect due to the use of ambient measurements instead of personal exposure. Extrapolation from citywide measurements to individual exposures can be problematic. In addition to exposure measurement error, gestational age is known to be measured with error on birth records. 29 Finally, as in previous studies, we could identify only conceptions resulting in a live birth; association between early pregnancy air pollution exposure and preterm birth would be underestimated if air pollution increased the risk of fetal loss in addition to preterm birth. Limited variability in air pollution levels may be another explanation for the absence of an effect in the present study. Despite differences in the pollutants and study design, several epidemiologic studies have reported weak evidence of an association between ambient air pollution level and preterm birth/LBW, beyond individual level characteristics. For example, maternal exposure to carbon monoxide or motor vehicle exhaust late in the pregnancy was associated with preterm birth/LBW in Canada and the United States. 12,25,30,31,32,33,34 Other studies have linked preterm birth/LBW to late pregnancy exposure to PM 2.5 and PM 10 in the Unites States and Brazil. 12,30,34,35 Early pregnancy exposure to ozone and PM 10 increased the risk of preterm delivery in Australia. 16 Increased concentrations of several pollutants during the 1 st and 3 rd trimesters were linked with preterm birth in the Republic of Korea. 36 A study from the Czech Republic found SO 2 to be associated with preterm birth regardless of period of exposure. 37 Another study from China reported that exposure to elevated level of SO 2 during the last trimester shortened gestational length 38 and contributed to LBW. 39 Additionally, exposure to particles during early gestation as well as to nitrogen oxides and nitrogen dioxide during early or late gestation was associated with preterm birth/LBW. 23,34,40 However, several studies have found no consistent association. In the Dutch Prevention and Incidence of Asthma and Mite Allergy (PIAMA) birth cohort, there was no significant association between preterm birth and NO 2 during the 1 st trimester, last month, or the entire pregnancy. 22 Neither was there any significant association between NO 2 and preterm birth in a study from the United States. 11 From Australia, an unexplained protective effect of NO 2 has been reported. 23 Several studies have found no association between exposure to CO, SO 2 , nitrogen dioxide, petrochemical pollutant, and the risk of LBW or small for gestational age. 41,42,43,44 The few studies conducted on ozone have not found robust associations. 11,16,23,25 Our estimated effect sizes for preterm birth/LBW may not be directly comparable to those from other air pollution studies because we estimated air pollution based on PSI. PSI may be a more appropriate metric than gas or particle mass concentration when evaluating health risk from air pollution. Ambient air pollution comprises a complex mixture of pollutants, and it is very difficult, if not impossible, to separate the effects of individual pollutants from those of others. The limitations of single pollutant models in explaining health consequences are increasingly recognized. 45,46 Expanding the number of pollutants measured in a study design is thus desirable. 46,47 However, we believe that it is likely that the linkage between preterm birth and temporal variations in ambient air pollution that we observed in this study was due to the mixture of air pollutants rather than just one component. It will be of significant interest to examine the impact of the interaction between these various measures and functional outcomes in pregnancy.

Although the exact mechanisms whereby air pollution is associated with higher risk of preterm birth/LBW are not entirely clear yet, several mechanisms, some of which may be specific to particular time windows in gestation, can be proposed. The weak association of air pollution with higher risk of preterm birth/LBW may be attributed to implantation errors in early pregnancy, oxidative stress, placental dysfunction, and inflammation, 48,49 which may increase the risk of preterm birth/LBW. There is evidence that in late pregnancy, maternal exposure to air pollution triggers inflammation that could increase maternal susceptibility to infections, which have been linked to uterine contractions and the initiation of preterm birth. 49,50 The component chemicals of air pollution can lead to systemic oxidative stress, resulting in DNA damage that has been linked to restricted fetal growth and lower birth weights. 49,50 Air pollution may also restrict fetal growth by causing placental dysfunction and subsequent nutrient and oxygen delivery to the fetus. 31 Reduced placental perfusion may result from inflammation 36,49 and increased blood viscosity 50 associated with maternal exposure to air pollution. Likewise, the crucial windows of exposure are not clear yet. The 1 st trimester exposure and the exposures during the 3 rd trimester and the last weeks preceding birth have been implicated as the most relevant. 11 Air pollution levels in the weeks following conception could disrupt implantation and placentation and increase the risk of preterm birth through suboptimal placental function. Maternal exposure to air pollution in a later stage of gestation may cause disturbances in cord blood flow or increased susceptibility for maternal infections, which may cause premature rupture of membranes leading to an earlier birth. 30 While a number of plausible pathways related to these mechanisms, particularly inflammation and implantation error, have been proposed, the mechanisms underlying the observed associations remain unclear, both because of the complex nature of preterm birth/LBW etiology as well as the heterogeneous composition of air pollution.

This study had several limitations. One potential source of bias is residual confounding due to the risk factors that we were unable to account for in our analysis (socio-economic status, educational level, air conditioning use, proximity to roadways, geographic location, level of physical activity, smoking, stress, nutrition, work environment, and maternal weight gain). Moreover, unknown confounders cannot be adjusted for. Thus, the observed minimal increased risk of preterm birth associated with air pollution may reflect confounding by these risk factors.

Furthermore, we assumed that ambient air pollution, measured by PSI, was spatially homogeneous within a geographic area around each monitor site. We also assumed that the mothers did not move during pregnancy. Finally, ambient air pollution levels were used as a surrogate measure for actual personal air pollution exposure. Our exposure estimates were based only on residential addresses, ignoring other microenvironments that might be important for personal exposure. Ritz et al. 11 reported the associations between monitor-based estimates of air pollution exposure during pregnancy and preterm birth to be greater for women who did not work (and for whom a residence-based measure of exposure presumably is more accurate) than for women who worked outside their homes.

In conclusion, the results from this study support a weak positive association between maternal exposure to ambient air pollution during the entire pregnancy and preterm birth. These associations are probably due to confounding factors, because of the observational design of our study. Further studies are warranted to find out more about these associations and possible mechanisms.

This work was partially supported by funds from Isfahan University of Medical Sciences, Iran. This research was performed as a part of the academic activity of the university.

Authors′ contributions

Janghorbani M. conceived the study aims and design, contributed to the discussion and revision of the manuscript, and drafted the manuscript. Piraei E. contributed to data collection, performed the analysis, and revised the manuscript. All authors discussed the results and reviewed and edited the manuscript.

Heron M Hoyert DL Murphy SL Xu J Kochanek KD Tejada-Vera B Deaths: final data for 2006.Natl Vital Stat Rep 2009 ;57 1 134 Mathews TJ MacDorman MF Infant mortality statistics from the 2004 period linked birth/infant death data setNatl Vital Stat Rep 2007 55 1 32 Behrman RE Butler AS (Eds )Preterm Birth: Causes, consequences, and prevention ) Preterm Birth: Causes, consequences, and prevention Institute of Medicine (US) Committee on Understanding Premature Birth and Assuring Healthy Outcomes; Washington (DC): National Academies Press (US); 2007 Lowdermilk D Perry S Bobak I Maternity and Women′s Health care.StLouis, Missouri: Mosby; 7 Maternity and Women's Health care St Louis, Missouri: Mosby; 2007 P 932-4 Escobar GJ Clark RH Greene JD Short-term outcomes of infants born at 35 and 36 weeks gestation: We need to ask more questionsSemin Perinatol 2006 30 28 33 Behman RE Butler AS editors Preterm birth: Cause, consequences, and prevention/ Committee on Understanding Premature Birth and Assuring Healthy Outcome, Board on Health Sciences PolicyWashington: National Academies Press; 7 Preterm birth: Cause, consequences, and prevention/ Committee on Understanding Premature Birth and Assuring Healthy Outcome, Board on Health Sciences Policy Washington: National Academies Press; 2007 Mangham LJ Petrou S Doyle LW Draper ES Marlow N The cost of preterm birth throughout childhood in England and WalesPediatrics 2009 123 e312 27 Cuevas KD Silver DR Brooten D Youngblut JM Bobo CM The cost of prematurity: Hospital charges at birth and frequency of rehospitalizations and acute care visits over the first year of life: A comparison by gestational age and birth weightAm J Nurs 2005 105 56 64 Petrou S The economic consequences of preterm birth during the first 10 years of lifeBJOG 2005 112(suppl 1) S10 5 Mattison DR Wilson S Coussens C D Gilbert The Role of Environmental Hazards in Premature BirthWashington, DC: National Academies Press; 3 The Role of Environmental Hazards in Premature Birth Washington, DC: National Academies Press; 2013 Ritz B Wilhelm M Hoggatt KJ Ghosh JK Ambient air pollution and preterm birth in the environment and pregnancy outcomes study at the University of California, Los AngelesAm J Epidemiol 2007 166 1045 52 Wilhelm M Ritz B Local variations in CO and particulate air pollution and adverse birth outcomes in Los Angeles County, California, USAEnviron Health Perspect 2005 113 1212 21 Sagiv SK Mendola P Loomis D Herring AH Neas LM Savitz DA A time-series analysis of air pollution and preterm birth in Pennsylvania, 1997-2001Environ Health Perspect 2005 113 602 6 Huynh M Woodruff TJ Parker JD Schoendorf KC Relationships between air pollution and preterm birth in CaliforniaPaediatr Perinat Epidemiol 2006 20 454 61 Brauer M Lencar C Tamburic L Koehoorn M Demers P Karr C A cohort study of traffic-related air pollution impacts on birth outcomesEnviron Health Perspect 2008 116 680 6 Hansen C Neller A Williams G Simpson R Maternal exposure to low levels of ambient air pollution and preterm birth in Brisbane, AustraliaBJOG 2006 113 935 41 Glinianaia SV Rankin J Bell R Pless-Mulloli T Howel D Particulate air pollution and fetal health: A systematic review of the epidemiologic evidenceEpidemiology 2004 15 36 45 Lacasana M Esplugues A Ballester F Exposure to ambient air pollution and prenatal and early childhood health effectsEur J Epidemiol 2005 20 183 99 Maisonet M Correa A Misra D Jaakkola JJ A review of the literature on the effects of ambient air pollution on fetal growthEnviron Res 2004 95 106 15 Sram RJ Binkova B Dejmek J Bobak M Ambient air pollution and pregnancy outcomes: A review of the literatureEnviron Health Perspect 2005 113 375 82 Stillerman KP Mattison DR Giudice LC Woodruff TJ Environmental exposures and adverse pregnancy outcomes: A review of the scienceReprod Sci 2008 15 631 50 Gehring U Wijga AH Fischer P de Jongste JC Kerkhof M Koppelman GH Traffic-related air pollution, preterm birth and term birth weight in the PIAMA birth cohort studyEnviron Res 2011 1111 125 35 Jalaludin B Mannes T Morgan G Lincoln D Sheppeard V Corbett S Impact of ambient air pollution on gestational age is modified by season in Sydney, AustraliaEnviron Health 2007 6 16 Darrow LA Klein M Flanders WD Waller LA Correa A Marcus M Ambient air pollution and preterm birth: A time-series analysisEpidemiology 2009 20 689 98 Liu S Krewski D Shi Y Chen Y Burnett RT Association between gaseous ambient air pollutants and adverse pregnancy outcomes in Vancouver, CanadaEnviron Health Perspect 2003 111 1773 8 Gehring U van Eijsden M Dijkema M van der Wal MF Fischer P Brunekreef B Traffic-related air pollution and pregnancy outcomes in the Dutch ABCD birth cohort studyOccup Environ Med 2011 68 36 43 van den Hooven EH Jaddoe VW de Kluizenaar Y Hofman A Mackenbach JP Steegers EA Residential traffic exposure and pregnancy-related outcomes: A prospective birth cohort studyEnviron Health 2009 8 59 Bosetti C Nieuwenhuijsen MJ Gallus S Cipriani S La Vecchia C Parazzini F Ambient particulate matter and preterm birth or birth weight: A review of the literatureArch Toxicol 2010 84 447 60 Wier ML Pearl M Kharrazi M Gestational age estimation on United States live birth certificates: A historical overviewPaediatr Perinat Epidemiol 2007 21(suppl 2) 4 12 Ritz B Yu F Chapa G Fruin S Effect of air pollution on preterm birth among children born in Southern California between 1989 and 1993Epidemiology 2000 11 502 11 Ritz B Yu F The effect of ambient carbon monoxide on low birth weight among children born in southern California between 1989 and 1993Environ Health Perspect 1999 107 17 25 Maisonet M Bush TJ Correa A Jaakkola JJ Relation between ambient air pollution and low birth weight in the Northeastern United StatesEnviron Health Perspect 2001 109 351 6 Salam MT Millstein J Li Y Lurmann FW Margolis HG Gilliland FD Birth outcomes and prenatal exposure to ozone, carbon monoxide, and particulate matter: Results from the children′s health studyEnviron Health Perspect 2005 113 1638 44 Bell ML Ebisu K Belanger K Ambient air pollution and low birth weight in Connecticut and MassachusettsEnviron Health Perspect 2007 115 1118 24 Ghosh R Rankin J Pless-Mulloli T Glinianaia S Does the effect of air pollution on pregnancy outcomes differ by gender.A systematic review?Environ Res 2007 105 400 8 Leem JH Kaplan BM Shim YK Pohl HR Gotway CA Bullard SM Exposures to air pollutants during pregnancy and preterm deliveryEnviron Health Perspect 2006 114 905 10 Bobak M Outdoor air pollution, low birth weight, and prematurityEnviron Health Perspect 2000 108 173 6 Xu X Ding H Wang X Acute effects of total suspended particles and sulfur dioxides on preterm delivery: A community-based cohort studyArch Environ Health 1995 50 407 15 Wang X Ding H Ryan L Xu X Associations between air pollution and low birth weight: A community-based studyEnviron Health Perspect 1997 105 514 20 Gouveia N Bremner SA Novaes HM Association between ambient air pollution and birth weight in Sao Paulo, BrazilJ Epidemiol Commun Health 2004 58 11 7 Marozine L Grazuleviciene R Maternal exposure to low-level air pollution and pregnancy outcomes:a population based studyEnviron Health 2002 1 6 Woodruff TJ Parker JD Kyle AC Schoendorf KC Disparities in exposure to air pollution during pregnancyEnviron Health Perspect 2003 111 942 6 Oliveira LM Stein N Sanseverino MT Vargas VM Fachel JM Schuler L Reproductive outcomes in an area adjacent to a petrochemical plant in southern BrazilRev Saude Publica 2002 36 81 7 Dolk H Pattenden S Vrijheid M Thakrar B Armstrong B Perinatal and infant mortality and low birth weight among residents near cokeworks in Great BritainArch Environ Health 2000 55 26 30 Sahsuvaroglu T Jerrett M Sources of uncertainty in calculating mortality and morbidity attributable to air pollutionJ Toxicol Environ Health A 2007 70 243 60 Mauderly JL Burnett RT Castillejos M Ozkaynak H Samet JM Stieb DM Is the air pollution health research community prepared to support a multipollutant air quality management framework.Inhal Toxicol 2010;22 (Suppl?):- 9 Is the air pollution health research community prepared to support a multipollutant air quality management framework Inhal Toxicol 2010;22 (Suppl 1):1-19 Dominici F Peng RD Barr CD Bell ML Protecting human health from air pollution: Shifting from a single-pollutant to a multipollutant approachEpidemiology 2010 21 187 94 Institute of Medicine of the National Academies Preterm Birth Causes, Consequences and PreventionWashington, DC: National Academies Press; 7 Preterm Birth Causes, Consequences and Prevention Washington, DC: National Academies Press; 2007 Kannan S Misra DP Dvonch JT Krishnakumar A Exposures to airborne particulate matter and adverse perinatal outcomes: A biologically plausible mechanistic framework for exploring potential effect modification by nutritionEnviron Health Perspect 2006 114 1636 42 Landgren O Environmental pollution and delivery outcome in southern Sweden: A study with central registriesActa Paediatr 1996 85 1361 4