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Prenatal Air Pollution Exposure, Smoking, and Uterine Vascular

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Prenatal Air Pollution Exposure, Smoking, and Uterine Vascular ISEE ENVIRONMENTAL Original Research EPIDEMIOLOGY Prenatal air pollution exposure, smoking, and uterine vascular resistance Zuelma A. Contrerasa, Julia E. Hecka, Pei-Chen Leeb, Xin Cuia, Calvin J. Hobelc, Carla Janzend, Fred Lurmanne, Beate Ritza 06/21/2018 on BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3yRlXg5VZA8sVKTq411E+1pYOm77OhO+8K8c6gR42unRN9KnLIQH6qA== by https://journals.lww.com/environepidem from Downloaded Downloaded Background: Prenatal exposure to air pollution and smoking increases the risk of pregnancy complications and adverse birth from outcomes, but pathophysiologic mechanisms are still debated. Few studies to date have examined the influence of air pollution on https://journals.lww.com/environepidem uterine vascular resistance, and no studies have examined the independent impact of these exposures. We aimed to assess the impact of prenatal exposure to traffic-related air pollution and smoking on uterine vascular resistance. Methods: Our study included 566 pregnant women recruited between 1993 and 1996 in Los Angeles who completed visits at three gestational ages. Information on smoking was collected, and uterine vascular resistance was measured at each visit by Doppler ultrasound. We calculated three resistance indices: the resistance index, the pulsatility index, and the systolic/diastolic ratio. We estimated exposure to NO2 at the home address of the mother using a land use regression model and to nitrogen oxides using CALINE4 air dispersion modeling. We used generalized linear mixed models to estimate the effects of air pollution and smoking on by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3yRlXg5VZA8sVKTq411E+1pYOm77OhO+8K8c6gR42unRN9KnLIQH6qA== uterine vascular resistance indices. Results: Land use regression–derived NO2 and CALINE4-derived nitrogen oxides exposure increased the risk of high uterine artery resistance in late pregnancy. Smoking during pregnancy also increased the risk of higher uterine resistance and contributed to bilat- eral notching in mid-pregnancy. Conclusion: Our results suggest that uterine vascular resistance is a mechanism underlying the association between smoking and air pollution and adverse birth outcomes. Key Words: uterine vascular resistance, smoking, air pollution, nitrogen dioxide, nitrogen oxide, resistance index Introduction has also been consistently associated with a number of adverse Maternal exposure to air pollution during pregnancy has been birth outcomes (fetal growth restriction, preterm birth, stillbirth) and pregnancy complications (placental abruption, placenta pre- linked to several adverse birth outcomes, including low birth 6 weight and preterm and small for gestational age births.1 Studies via, spontaneous abortions, ectopic pregnancies). Interestingly, smoking has been found to reduce risk of preeclampsia, though have also found an increased risk of gestational hypertension and 6,7 preeclampsia with prenatal air pollution exposure.2,3 Maternal the mechanisms for this are not well understood. Thus, further hypertensive disorders and intrauterine growth restriction are studies that aim to examine the impact of smoking on placental hypothesized to share common pathways as both are character- development and function are needed. ized by abnormal placental implantation and subsequent inad- Doppler ultrasound has long been used to assess uterine resis- equate uteroplacental blood flow.4,5 Smoking during pregnancy tance to blood flow and to register the presence of “notching” in the uterine arteries. In nonpregnant women and in early preg- nancy, blood flow in the uterine arteries typically has a high sys- aDepartment of Epidemiology, Fielding School of Public Health, University of tolic and low diastolic flow profile, with the presence of an early California, Los Angeles, CA, USA; bDepartment of Health Care Management, diastolic “notch” seen on Doppler ultrasound. As normal preg- College of Health Technology, National Taipei University of Nursing and Health nancy progresses, uterine resistance to blood flow decreases and Sciences, Taipei, Taiwan; cDepartment of Obstetrics, Gynecology and Pediatrics, the notch disappears around 18–24 weeks of gestation. Two com- Cedars Sinai Medical Center, Los Angeles, California, USA; dDepartment of monly used blood flow resistance indices are the pulsatility index Obstetrics and Gynecology, David Geffen School of Medicine, University of on e (PI; peak systolic flow minus end diastolic flow divided by mean 06/21/2018 California, Los Angeles, California, USA; Sonoma Technology, Inc., Petaluma, California, USA. Supplemental digital content is available through direct URL citations in the HTML and PDF versions of this article (www.epidem.com). What this study adds Correspondence author. Address: Beate Ritz, Department of Epidemiology, 650 Though there is convincing evidence from epidemiological Charles E. Young Drive, Box 951772, Los Angeles, CA 90095–1772. studies that air pollution exposure is associated with negative E-mail: [email protected] pregnancy outcomes, the physiologic mechanisms underlying Copyright © 2018 The Authors. Published by Wolters Kluwer Health, Inc. on these relations are largely unknown. Our study suggests that behalf of Environmental Epidemiology. All rights reserved. This is an open-access increased resistance to blood flow in the uterine arteries during article distributed under the terms of the Creative Commons Attribution-Non pregnancy may be one such mechanism. This finding could Commercial-No Derivatives License 4.0, where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any help expand our understanding of the potentially causal rela- way or used commercially. tion between air pollution exposure and adverse pregnancy outcomes. Furthermore, smoking during pregnancy appears to Environmental Epidemiology (2018) 2:e017 have a similar detrimental impact on blood flow in the uterine Received: 18 November 2017; Accepted 3 May 2018 arteries affecting pregnancy earlier in gestation, highlighting the Published online 21 June 2018 importance of considering both the effects of smoking and air DOI: 10.1097/EE9.0000000000000017 pollution on pregnancy. 1 Contreras et al. • Environmental Epidemiology (2018) 2:e017 Environmental Epidemiology flow) and the resistance index (RI; peak systolic flow minus end Doppler measurements were performed on the left and right diastolic flow divided by peak systolic flow), with higher values proximal uterine artery at each visit. Measurements on each denoting a lower diastolic flow.8,9 High uterine flow resistance uterine artery were obtained to the point near the cross-over and notching have clinical relevance in mid-to-late pregnancy as with the external iliac artery. For each waveform, the peak sys- they have been shown to be predictive of a range of pregnancy tolic (S) and end diastolic (D) velocities were measured three complications and adverse fetal outcomes, most notably pre- times, and the mean value of these three measurements were eclampsia and intrauterine growth restriction.8,10–13 calculated. We calculated three related flow indices: the PI, the It is plausible that air pollution contributes to impaired RI, and the systolic/diastolic (S/D) ratio.26,27 We found no dif- uterine vascular resistance as studies have shown that air pol- ference between left and right uterine artery resistance indices; lution upregulates endothelin, a vasoconstrictor, and increases thus, we averaged values for both sides (left and right uterine plasma viscosity, though no studies have examined this specifi- artery RI) at each visit for each participant as previously done in cally in pregnant women.14,15 Furthermore, animal studies have this cohort.12 The presence of uterine notching was also assessed also shown that air pollution can cause changes in placental at each visit. morphology that could contribute to decreased uteroplacental blood flow.16 Studies on prenatal air pollution and uterine vas- cular resistance are limited, with only two studies having exam- Traffic-related air pollution exposure 14,17 ined this to date. One study in the Netherlands found an Exposures to traffic-related air pollutants were assessed at association between NO2 exposure and third-trimester uterine participants’ residential address reported at baseline (visit 1). bilateral notching, but no associations between PM10 and NO2 Addresses were geocoded using three methods including (1) exposure and uterine artery resistance in the second and third geocoded to the parcel level using the TeleAtlas Address Point trimester. The other study, conducted in Brazil, examined uterine database (n = 404); (2) geocoded using address interpolation artery resistance in relation to NO2 and O3 exposure and found via the TeleAtlas EZ Locate geocoding service (n = 117); and no associations. (3) geocoded using Google Earth (n = 38), equivalent to highest The impact of smoking during pregnancy on uterine vascu- quality matching using EZ Locate). Seven addresses could not lar resistance has been more frequently studied, with studies be mapped, resulting in missing air pollution assignments. finding some support for an increased vascular resistance in the uterine arteries in response to maternal smoking, but the evi- dence is inconclusive.18–22 It is plausible that smoking results in CALINE4 nitrogen oxides exposure estimates reduced blood flow as smoking has been shown to cause struc- We used the CALINE4 line dispersion model,28,29
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