Wildfire Smoke Exposure during Pregnancy: A Review of Potential Mechanisms of Placental Toxicity, Impact on Obstetric Outcomes, and Strategies to Reduce Exposure
Abstract
:1. Introduction
1.1. The Complexity of Wildfire Smoke Composition
1.2. Wildfire Smoke, PM2.5, and Impact on Perinatal Outcomes
1.2.1. Preterm Birth
1.2.2. Fetal Growth
Citation | Type of Exposure | Time | Location | Study Design | Study Population | Sample Size (n) | Description of Exposure | Primary Outcome(s) | Secondary Outcome(s) |
---|---|---|---|---|---|---|---|---|---|
Abdo (2019) [29] | Wildfire smoke | 2007–2015 | Colorado, USA | Retrospective cohort | Singleton births with estimated gestational age between 30 and 42 weeks | 446,961 | Wildfire smoke PM2.5 and non-smoke PM2.5 linked by maternal residence ZIP code; method combined NOAA’s satellite imagery-based HMS to determine daily smoke plume extent with spatial interpolation of ground-based PM2.5 monitor values from US EPA AQS | PTB, BW | NICU admission, gestational diabetes, gestational hypertension, assisted ventilation at |
Assibey-Mensah (2020) [39] | Wood smoke and traffic particle pollution | 2009–2013 | New York, USA | Retrospective cohort | Birth certificate data with gestation age estimated between 24 and 42 weeks | 20,596 | PM2.5, black carbon, Delta-C (wood smoke marker) concentrations, temperature, and relative humidity measured hourly, gestational month-specific concentrations of each at maternal residential address estimated using land-use regression model | Preeclampsia, any type (early- and late-onset) | |
Breton (2011) [38] | Wildfire smoke | 2003–2004 | California, USA | Retrospective cohort | Pregnant women living in southern California | Not reported | Wildfire PM2.5 and ambient PM2.5 assigned exposures from maternal addresses geocoded for week of wildfire, exposure estimates derived in a GIS framework, MODIS satellite imaging used to obtain smoke information | BW | SGA, PTB |
Heft-Neal (2022) [30] | Wildfire smoke | 2006–2012 | California, USA | Retrospective cohort | Singleton births in California with estimated gestation age between 23 and 41 weeks | 3,002,014 | Wildfire smoke plume extent assembled from NOAA’s satellite imagery-based HMS, high-resolution, temporally and spatially resolved gridded estimates of surface PM2.5 developed using machine learning algorithms to incorporate ground monitor data, chemical transport model predictions, and satellite observations; exposures linked to maternal address ZIP code | PTB | PTB subtype and severity (<28 weeks, <32 weeks) |
Holstius (2012) [35] | Wildfire smoke | 2001–2005 | California, USA | Time-series | Birth records from the California Automated Vital Statistics System for infants delivered at term with BW between 1–6 kg | 886,034 | Temporally defined smoke exposure from MODIS satellite imagery, sensitivity analysis using maternal residence census tracts closer to monitors with average PM10 of <40 µg/m3 classified as low exposure, >40 µg/m3 classified as high exposure. | BW | |
Jayachandran (2009) [40] | Wildfire air pollution | 1997 | Sumatra, Indonesia | Ecological | Birth cohorts conceived before or after wildfire events | 3751 | TOMS aerosol index | Fetal loss, infant mortality | |
McCoy (2016) [37] | Wildfire smoke | 2002–2013 | Colorado, USA | Retrospective cohort | Live births in Colorado with maternal home address within 20 miles of a fire burn and smoke plume | 7398 | Proximity of self-reported maternal residence to wild-fire smoke using fine-scaled spatial dataset of plumes in GIS from satellite images of 28 wildfires in Colorado | BW, GA | |
O’Donnell (2013) [34] | Wildfire event | 2009 | Victoria, Australia | Retrospective cohort | All births registered in Victoria | 287,688 | Proximity of maternal residence to Black Saturday wildfires | BW, PTB, changes to sex-ratio | |
O’Donnell (2015) [32] | Wildfire event | 2000–2010 | Canberra, Australia | Retrospective cohort | All births registered in Canberra | 48,408 | Proximity of maternal residence to wildfire | BW, GA | |
Prass (2012) [36] | Forest fire event | 2001–2006 | Porto Velho, Brazil | Cross- sectional | Singleton live births | 22,012 | Heat spots (all forest fires in Amazon region from 2001–2006) compared to time periods with lowest numbers of heat spots using NOAA satellite images | BW |
1.3. Anatomy of the Human Maternal-Fetal Interface and Particulate Matter Deposition
1.4. Biologic Mechanisms of Damage from Wildfire, Air Pollution and Inhaled Toxins
1.4.1. Inflammation
1.4.2. Oxidative Stress
1.4.3. Endocrine Dysfunction
1.4.4. Hemodynamic and Vascular Function
1.4.5. Coagulation
1.4.6. Epigenetic Alterations
1.4.7. Telomere Length
2. Review of the Current Human, Animal and Placental Studies
2.1. Exposure Reduction Strategies and Implications for Research
2.1.1. Behavioral Modifications, Air Filters, and Masks
2.1.2. Personal Air Quality Monitors
2.1.3. Implications for Research
3. Discussion
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
CO | carbon monoxide |
CTB | cytotrophoblasts |
HEPA | high efficiency particulate air |
NO2 | nitrogen dioxide |
OS | oxidative stress |
O3 | ozone |
PM | particulate matter |
PM2.5 | particulate matter < 2.5 µm |
PM10 | particulate matter < 10 µm |
PAH | polycyclic aromatic hydrocarbon |
PTB | preterm birth |
ROS | reactive oxygen species |
STB | syncytiotrophoblasts |
US | United States (US) |
WS | wildfire smoke |
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Citation | Type of Exposure | Time | Location | Animal Model | Sample Source(s) | Sample Size (n) | Description of Exposure | Primary Outcome(s) |
---|---|---|---|---|---|---|---|---|
Black (2017) [26] | Wildfire smoke | 2008 | California, USA | Adult female rhesus macaque (Macaca mulatta) exposed in infancy to wildfire season in 2008 | Blood | 50 | Ozone and PM2.5 concentrations from air monitoring stations | PBMC in vitro challenge testing, cytokine protein assay 6 h after TLR ligand addition, IL-6 and IL-8 levels, Pulmonary function measures |
Brown (2022) [76] | Wildfire smoke | 2008–2009 | California, USA | Adult female rhesus macaque (Macaca mulatta) exposed in their first three months of life to wildfire season in 2008 | Nasal epithelium, peripheral blood | 22 | Wildfire smoke PM2.5, ozone exposure during early life | Whole genome bisulfite sequencing to identify differentially methylated regions from nasal epithelium, RNA-sequencing on a subset of samples |
Capitano (2022) [74] | Wildfire smoke | 2018 | California, USA | Infant female rhesus macaque (Macaca mulatta) | --- | 56 | Mean daily PM2.5 | BioBehavioral Assessment, CRP levels via high sensitivity assay, cortisol concentration via I125 radioimmunoassay |
Detmar (2008) [72] | Polycyclic aromatic hydrocarbons | 2008 | Toronto, Canada | C57BI/6 female mice | Placenta, fetus | 4 | Subcutaneous injections of PAH over a 9-week period | Fetal growth, placental cell death rates, expression of antiapoptotic Xiap, proapoptotic Bax, levels of cleaved poly(ADP-ribose) polymerase-, and active caspase-3 |
Hong (2013) [152] | Particulate matter | 2012 | Fujian, China | Mouse | Blood, spleen, thymus | 40 | Instillation of airborne PM solution into mouse lung | IL-4 and IFN-γ levels in plasma and spleen, splenic lymphocyte proliferation, GATA-3 and T-bet mRNA in spleen tested, histopathology of spleen and thymus. |
Lee (2015) [153] | Environmental tobacco smoke | 2015 | California and Montana, USA | Mouse | Bronchial alveolar lavage fluid | 4 | Tobacco smoke (1.0 mg/m3) for 6 h/day | Global DNA methylation, cytokine measurements |
Valentino (2016) [111] | Diesel engine exhaust | 2016 | France | New-Zealand white female rabbits (INRA1077 line) | Maternal lung, maternal and fetal plasma, placenta, fetus | 28 | Inhalation of diesel exhaust from 3rd to 27th day post-conception (20 days over 31 day gestation) | Ultrasound with biometry and Doppler monitoring, birth weight, TEM of lung, vascular and placental tissue to identify NPs |
Miller (2020) [107] | Ozone | 2020 | North Carolina, USA | Long-Evans rat | Placenta, fetus | 8 | Gaseous ozone for 4 h in the mornings of gestation days 5 and 6 (during implantation) | DNA and RNA expression from placenta, hepatic gene expression, mitochondrial respiration, metabolic assessment |
Zhu (2021) [99] | PM2.5 | 2021 | Taiguan, China | C57BL/6 mice | Placenta, fetus | 55 | Oropharyngeal aspiration of PM2.5 every other day starting on embryonic day 0.5 | Expression of proliferating cell nuclear antigen, mRNA of amino acids, long-chain polyunsaturated fatty acid, glucose, glycogen, triglycerides, and folate transporters |
Citation | Type of Exposure | Time | Location | Study Population | Sample Source(s) | Sample Size (n) | Description of Exposure | Primary Outcome(s) |
---|---|---|---|---|---|---|---|---|
Abraham (2018) [146] | Air pollution | 2003–2006 | France | Singleton pregnancies enrolled before 24 weeks of gestation | Placenta samples collected at delivery | 688 | NO2 and PM10 hourly concentrations modelled using maternal home address, mean daily temperature and humidity from nearest stationary monitors | Genome-wide DNA placental methylation levels |
Adebambo (2018) [154] | Cadmium treatment | 2018 | Longjiang River, China | JEG-3 choriocarcinoma cell line | Placental trophoblast cells | 6 | Environmental water samples from a cadmium spill site in China | Reactive oxygen species (ROS), expression of metallothionein (MT) isoforms, HIF1α, and TGFβ associated genes and proteins |
Arita (2022) [89] | Dimethylaniline (DMA) | 2022 | New York, New Jersey, USA | Placental explants | Placental explant cultures from term placentas collected from elective cesarean sections | 12 | DMA instilled into placental explant well plates to final concentrations of 0–50 μM | IL-1β, TNF-α, IL-6, sgp130, IL-10, BDNF, HO-1, 8-IsoP, P4, T, E2 quantification using immunoassay reagents |
Basilio (2021) [68] | Wildfire smoke | 2018–2019 | California | Mid gestation placenta | First and second trimester placenta from elective terminations of pregnancy | 12 | Average daily AQI levels during gestation | Fetal Hofbauer cells (CD68+) |
Bové (2019) [49] | Air pollution | 2012–2016 | Belgium | ENVIRONAGE birth cohort, singleton births recruited on arrival for delivery | Term and preterm placenta collected within 10 min after birth | 10 | Ambient exposure to BC determined using maternal residential address using spatial and temporal integration from satellite images and pollution data from fixed monitoring stations | Detection of BC particles, BC load |
Bainbridge (2006) [115] | Carbon monoxide | 2006 | Canada | Placental explants | Placental explant cultures from term placentas collected from elective cesarean sections | 13 | Carbon monoxide infused culture medium | Apoptotic Index using TUNEL assay, Immunohistochemical staining for p85 Fragment of PARP, morphology of villous tissue, villous tissue integrity |
Erlandsson (2020) [51] | Wood smoke | 2020 | Sweden | First trimester trophoblast cell line HTR-8 | HTR-8 was derived by transfecting cells from chorionic villi explants from placentas of 6–12 week gestation | 6-well plates | Smoke burned on wood stove from logs of four different species (silver birch, quaking aspen, Norway spruce, and Scots pine) at a nominal burn rate and high burn rate, wood particles collected and extracted then aliquoted into well plates | hCG, progesterone and IL-6; cellular particle localization and uptake by TEM, cytotoxicity assay, PAH analysis, membrane integrity testing |
Janssen (2012) [155] | Air pollution | 2012–2016 | Belgium | ENVIRONAGE birth cohort, singleton births recruited on arrival for delivery | Human, placenta and cord blood | 174 | PM10 incremental exposure | mtDNA content |
Janssen (2013) [156] | Air pollution | 2012–2016 | Belgium | ENVIRONAGE birth cohort, singleton births recruited on arrival for delivery | Human, placenta | 240 | PM2.5 incremental exposure | Global DNA methylation |
Janssen (2015) [157] | Air pollution | 2012–2016 | Belgium | ENVIRONAGE birth cohort, singleton births recruited on arrival for delivery | Human, placenta | 381 | PM2.5 incremental exposure | mtDNA methylation |
Saenen (2015) [57] | Air pollution | 2012–2016 | Belgium | ENVIRONAGE birth cohort, singleton births recruited on arrival for delivery | Human, placenta | 90 | PM2.5 incremental exposure | Gene expression in BDNF and SYN1 pathways |
Saenen (2016) [91] | Air pollution | 2012–2016 | Belgium | ENVIRONAGE birth cohort, singleton births recruited on arrival for delivery | Human, placenta | 336 | PM2.5 incremental exposure | 3-nitrotyrosine |
Prevention of WS Exposure |
---|
(1) Stay indoors with a high-efficiency air filter * |
(2) Seek shelter with a high-efficiency air filter * |
(3) Use N95 respirator or P100 respirator |
(4) Reduce outdoor exposure |
(5) Reduce strenuous activities to reduce inhalation |
(6) Evacuate safely and prepare an evacuation kit with food, water, and medications for 7–10 days, first aid supplies and important documents |
(7) Do not consume any food, beverages, or medications that have been exposed to burn debris or ash; avoid using wood-burning stoves, fireplaces, gas, propane, or vacuum |
(8) Protect pets by keeping them indoors. If you must evacuate without your pets, never tie them up |
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Basilio, E.; Chen, R.; Fernandez, A.C.; Padula, A.M.; Robinson, J.F.; Gaw, S.L. Wildfire Smoke Exposure during Pregnancy: A Review of Potential Mechanisms of Placental Toxicity, Impact on Obstetric Outcomes, and Strategies to Reduce Exposure. Int. J. Environ. Res. Public Health 2022, 19, 13727. https://doi.org/10.3390/ijerph192113727
Basilio E, Chen R, Fernandez AC, Padula AM, Robinson JF, Gaw SL. Wildfire Smoke Exposure during Pregnancy: A Review of Potential Mechanisms of Placental Toxicity, Impact on Obstetric Outcomes, and Strategies to Reduce Exposure. International Journal of Environmental Research and Public Health. 2022; 19(21):13727. https://doi.org/10.3390/ijerph192113727
Chicago/Turabian StyleBasilio, Emilia, Rebecca Chen, Anna Claire Fernandez, Amy M. Padula, Joshua F. Robinson, and Stephanie L. Gaw. 2022. "Wildfire Smoke Exposure during Pregnancy: A Review of Potential Mechanisms of Placental Toxicity, Impact on Obstetric Outcomes, and Strategies to Reduce Exposure" International Journal of Environmental Research and Public Health 19, no. 21: 13727. https://doi.org/10.3390/ijerph192113727