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Reductions in urinary metabolites of exposure to household air pollution in pregnant, rural Guatemalan women provided liquefied petroleum gas stoves

Journal of Exposure Science & Environmental Epidemiology volume 30, pages 362–373 (2020)Cite this article

Abstract

Background

Household air pollution from solid fuels is a leading risk factor for morbidity and mortality worldwide. Pregnant women’s exposure to polycyclic aromatic hydrocarbons (PAHs) and volatile organic compounds (VOCs), two components of solid-fuel smoke, is associated with adverse birth outcomes. Even with improved solid-fuel stoves, exposure to PAHs and VOCs remains high. Therefore, cleaner cooking fuels need to be prioritized.

Objective

We aimed to quantify exposure reduction to PAHs and VOCs among pregnant women in rural Guatemala with a liquefied petroleum gas (LPG) stove intervention.

Materials and methods

Urine from pregnant women (N = 50) was collected twice: at <20 weeks gestation, when women cooked exclusively with wood, and 6–8 weeks after receiving an LPG stove. Metabolites of four PAHs and eight VOCs were analyzed. Concurrent with urine collection, personal 48-h PM2.5 exposure was measured.

Results

Women cooking exclusively with wood were exposed to high levels of particulate matter (PM2.5), which was reduced by 57% with the LPG stove. Urinary concentrations of total PAH metabolites (−37%), PMA (benzene metabolite; −49%), and CNEMA (acrylonitrile metabolite; −51%) were reduced. However, recent use of a wood-fired sauna bath led to large increases in excretion of urinary toxicant metabolites (+66–135%).

Conclusions

This is the first study to report PAH and VOC reductions from an LPG stove intervention introduced during pregnancy. However, other sources of air pollution minimized the gains seen from using an LPG stove. Thus, all sources of air pollution must be addressed in concert to reduce exposures to levels that protect health.

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References

  1. IHME (Institute for Health Metrics and Evaluation). GBD Compare [Internet]. 2017. Available from: http://vizhub.healthdata.org/gbd-compare/

  2. WHO. Population using solid fuels (estimates): Data by country. Global Health Observatory data repository [Internet]. 2013 [cited 20 May 2016]; Available from: http://apps.who.int/gho/data/node.main.135?lang=en%E2%80%9D

  3. G. B. D. Risk Factors Collaborators, Forouzanfar MH, Alexander L, Anderson HR, Bachman VF, Biryukov S, et al. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks in 188 countries, 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2015;386:2287–323.

    Article  Google Scholar 

  4. Preker AS, Adeyi OO, Lapetra MG, Simon DC, Keuffel E. Health care expenditures associated with pollution: exploratory methods and findings. Ann Glob Health. 2016;82:711–21.

    Article  Google Scholar 

  5. Patelarou E, Kelly FJ. Indoor exposure and adverse birth outcomes related to fetal growth, miscarriage and prematurity-a systematic review. Int J Environ Res public Health. 2014;11:5904–33.

    Article  Google Scholar 

  6. Titcombe ME, Simcik M. Personal and indoor exposure to PM(2).(5) and polycyclic aromatic hydrocarbons in the southern highlands of Tanzania: a pilot-scale study. Environ Monit Assess. 2011;180:461–76.

    Article  CAS  Google Scholar 

  7. Vanker A, Barnett W, Nduru PM, Gie RP, Sly PD, Zar HJ. Home environment and indoor air pollution exposure in an African birth cohort study. Sci Total Environ. 2015;536:362–7.

    Article  CAS  Google Scholar 

  8. Shen G, Preston W, Ebersviller SM, Williams C, Faircloth JW, Jetter JJ, et al. Polycyclic aromatic hydrocarbons in fine particulate matter emitted from burning kerosene, liquid petroleum gas, and wood fuels in household cookstoves. Energy Fuels. 2017;31:3081–90.

    Article  CAS  Google Scholar 

  9. Choi H, Rauh V, Garfinkel R, Tu Y, Perera FP. Prenatal exposure to airborne polycyclic aromatic hydrocarbons and risk of intrauterine growth restriction. Environ Health Perspect. 2008;116:658–65.

    Article  CAS  Google Scholar 

  10. Padula AM, Noth EM, Hammond SK, Lurmann FW, Yang W, Tager IB, et al. Exposure to airborne polycyclic aromatic hydrocarbons during pregnancy and risk of preterm birth. Environ Res. 2014;135:221–6.

    Article  CAS  Google Scholar 

  11. Ren A, Qiu X, Jin L, Ma J, Li Z, Zhang L, et al. Association of selected persistent organic pollutants in the placenta with the risk of neural tube defects. Proc Natl Acad Sci USA. 2011;108:12770–5.

    Article  CAS  Google Scholar 

  12. Wang B, Jin L, Ren A, Yuan Y, Liu J, Li Z, et al. Levels of polycyclic aromatic hydrocarbons in maternal serum and risk of neural tube defects in offspring. Environ Sci Technol. 2015;49:588–96.

    Article  CAS  Google Scholar 

  13. Lupo PJ, Langlois PH, Reefhuis J, Lawson CC, Symanski E, Desrosiers TA, et al. Maternal occupational exposure to polycyclic aromatic hydrocarbons: effects on gastroschisis among offspring in the national birth defects prevention study. Environ Health Perspect. 2012;120:910–5.

    Article  CAS  Google Scholar 

  14. Langlois PH, Hoyt AT, Desrosiers TA, Lupo PJ, Lawson CC, Waters MA, et al. Maternal occupational exposure to polycyclic aromatic hydrocarbons and small for gestational age offspring. Occup Environ Med. 2014;71:529–35.

    Article  Google Scholar 

  15. Perera FP, Rauh V, Tsai WY, Kinney P, Camann D, Barr D, et al. Effects of transplacental exposure to environmental pollutants on birth outcomes in a multiethnic population. Environ Health Perspect. 2003;111:201–5.

    Article  CAS  Google Scholar 

  16. Tang D, Li TY, Chow JC, Kulkarni SU, Watson JG, Ho SS, et al. Air pollution effects on fetal and child development: a cohort comparison in China. Environ Pollut. 2014;185:90–6.

    Article  CAS  Google Scholar 

  17. Jedrychowski WA, Majewska R, Spengler JD, Camann D, Roen EL, Perera FP. Prenatal exposure to fine particles and polycyclic aromatic hydrocarbons and birth outcomes: a two-pollutant approach. Int Arch Occup Environ Health. 2017;90:255–64.

    Article  CAS  Google Scholar 

  18. Yang P, Gong Y-J, Cao W-C, Wang R-X, Wang Y-X, Liu C, et al. Prenatal urinary polycyclic aromatic hydrocarbon metabolites, global DNA methylation in cord blood, and birth outcomes: A cohort study in China. Environ Pollut. 2018;234:396–405.

    Article  CAS  Google Scholar 

  19. Perera F, Li TY, Zhou ZJ, Yuan T, Chen YH, Qu L, et al. Benefits of reducing prenatal exposure to coal-burning pollutants to children’s neurodevelopment in China. Environ Health Perspect. 2008;116:1396–400.

    Article  Google Scholar 

  20. Perera FP, Li Z, Whyatt R, Hoepner L, Wang S, Camann D, et al. Prenatal airborne polycyclic aromatic hydrocarbon exposure and child IQ at age 5 years. Pediatrics. 2009;124:e195–202.

    Article  Google Scholar 

  21. Sorensen M, Andersen AM, Raaschou-Nielsen O. Non-occupational exposure to paint fumes during pregnancy and fetal growth in a general population. Environ Res. 2010;110:383–7.

    Article  CAS  Google Scholar 

  22. Chang M, Park H, Ha M, Hong Y-C, Lim Y-H, Kim Y, et al. The effect of prenatal TVOC exposure on birth and infantile weight: the Mothers and Children’s Environmental Health study. Pediatr Res. 2017;82:423–8.

    Article  CAS  Google Scholar 

  23. Chang M, Lee D, Park H, Ha M, Hong Y-C, Kim Y, et al. Prenatal TVOCs exposure negatively influences postnatal neurobehavioral development. Sci Total Environ. 2018;618:977–81.

    Article  CAS  Google Scholar 

  24. Li Z, Sjodin A, Romanoff LC, Horton K, Fitzgerald CL, Eppler A, et al. Evaluation of exposure reduction to indoor air pollution in stove intervention projects in Peru by urinary biomonitoring of polycyclic aromatic hydrocarbon metabolites. Environ Int. 2011;37:1157–63.

    Article  CAS  Google Scholar 

  25. Riojas-Rodriguez H, Schilmann A, Marron-Mares AT, Masera O, Li Z, Romanoff L, et al. Impact of the improved patsari biomass stove on urinary polycyclic aromatic hydrocarbon biomarkers and carbon monoxide exposures in rural Mexican women. Environ Health Perspect. 2011;119:1301–7.

    Article  CAS  Google Scholar 

  26. Li Z, Commodore A, Hartinger S, Lewin M, Sjodin A, Pittman E, et al. Biomonitoring human exposure to household air pollution and association with self-reported health symptoms—a stove intervention study in Peru. Environ Int. 2016;97:195–203.

    Article  CAS  Google Scholar 

  27. Torres-Dosal A, Perez-Maldonado IN, Jasso-Pineda Y, Martinez Salinas RI, Alegria-Torres JA, Diaz-Barriga F. Indoor air pollution in a Mexican indigenous community: evaluation of risk reduction program using biomarkers of exposure and effect. Sci Total Environ. 2008;390:362–8.

    Article  CAS  Google Scholar 

  28. WHO. WHO Indoor Air Quality Guidelines: Household fuel combustion. Geneva: World Health Organization; 2014.

    Google Scholar 

  29. Weinstein JR, Asteria-Penaloza R, Diaz-Artiga A, Davila G, Hammond SK, Ryde IT, et al. Exposure to polycyclic aromatic hydrocarbons and volatile organic compounds among recently pregnant rural Guatemalan women cooking and heating with solid fuels. Int J Hyg Environ Health. 2017;220:726–35.

    Article  CAS  Google Scholar 

  30. Thompson LM, Diaz-Artiga A, Weinstein JR, Handley MA. Designing a behavioral intervention using the COM-B model and the theoretical domains framework to promote gas stove use in rural Guatemala: a formative research study. BMC Public Health. 2018;18:253.

    Article  Google Scholar 

  31. Ministerio de Salud Publica y Asistencia Social (MSPAS), Instituto Nacional de Estadistica (INE), Instituto Nacional de Estadistica International I. Encuestra de Salud Materno Infantil 2014–2015. Guatemala; 2017.

  32. WHO, IARC (International Agency for Research on Cancer). Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures. IARC Monogr Eval Carcinog Risks Hum. 2010;92:99–106.

  33. Alwis KU, Blount BC, Britt AS, Patel D, Ashley DL. Simultaneous analysis of 28 urinary VOC metabolites using ultra high performance liquid chromatography coupled with electrospray ionization tandem mass spectrometry (UPLC-ESI/MSMS). Anal Chim Acta. 2012;750:152–60.

    Article  CAS  Google Scholar 

  34. Jacob P 3rd, Wilson M, Benowitz NL. Determination of phenolic metabolites of polycyclic aromatic hydrocarbons in human urine as their pentafluorobenzyl ether derivatives using liquid chromatography-tandem mass spectrometry. Anal Chem. 2007;79:587–98.

    Article  CAS  Google Scholar 

  35. Lam N, Nicas M, Ruiz-Mercado I, Thompson LM, Romero C, Smith KR. Non-invasive measurement of carbon monoxide burden in Guatemalan children and adults following wood-fired temazcal (sauna-bath) use. J Environ Monit. 2011;13:2172–81.

    Article  CAS  Google Scholar 

  36. Carter E, Archer-Nicholls S, Ni K, Lai AM, Niu H, Secrest MH, et al. Seasonal and diurnal air pollution from residential cooking and space heating in the eastern Tibetan plateau. Environ Sci Technol. 2016;50:8353–61.

    Article  CAS  Google Scholar 

  37. Ni K, Carter E, Schauer JJ, Ezzati M, Zhang Y, Niu H, et al. Seasonal variation in outdoor, indoor, and personal air pollution exposures of women using wood stoves in the Tibetan Plateau: Baseline assessment for an energy intervention study. Environ Int. 2016;94:449–57.

    Article  CAS  Google Scholar 

  38. Benowitz NL, Gan Q, Goniewicz ML, Lu W, Xu J, Li X, et al. Different profiles of carcinogen exposure in Chinese compared with US cigarette smokers. Tob Control. 2015;24:e258–63.

    Article  Google Scholar 

  39. Pruneda-Alvarez LG, Perez-Vazquez FJ, Salgado-Bustamante M, Martinez-Salinas RI, Pelallo-Martinez NA, Perez-Maldonado IN. Exposure to indoor air pollutants (polycyclic aromatic hydrocarbons, toluene, benzene) in Mexican indigenous women. Indoor Air. 2012;22:140–7.

    Article  CAS  Google Scholar 

  40. Choi H, Wang L, Lin X, Spengler JD, Perera FP. Fetal window of vulnerability to airborne polycyclic aromatic hydrocarbons on proportional intrauterine growth restriction. PLoS ONE. 2012;7:e35464.

    Article  CAS  Google Scholar 

  41. St Helen G, Jacob P 3rd, Peng M, Dempsey DA, Hammond SK, Benowitz NL. Intake of toxic and carcinogenic volatile organic compounds from secondhand smoke in motor vehicles. Cancer Epidemiol Biomark Prev. 2014;23:2774–82.

    Article  Google Scholar 

  42. Thompson LM, Clark M, Cadman B, Canuz E, Smith KR. Exposures to high levels of carbon monoxide from wood-fired temazcal (steam bath) use in highland Guatemala. Int J Occup Environ Health. 2011;17:103–12.

    Article  CAS  Google Scholar 

  43. Lemieux PM, Lutes CC, Santoianni DA. Emissions of organic air toxics from open burning: a comprehensive review. Prog Energy Combust Sci. 2004;30:1–32.

    Article  CAS  Google Scholar 

  44. Li Z, Romanoff L, Bartell S, Pittman EN, Trinidad DA, McClean M, et al. Excretion profiles and half-lives of ten urinary polycyclic aromatic hydrocarbon metabolites after dietary exposure. Chem Res Toxicol. 2012;25:1452–61.

    Article  CAS  Google Scholar 

  45. McClean MD, Rinehart RD, Ngo L, Eisen EA, Kelsey KT, Wiencke JK, et al. Urinary 1-hydroxypyrene and polycyclic aromatic hydrocarbon exposure among asphalt paving workers. Ann Occup Hyg. 2004;48:565–78.

    CAS  Google Scholar 

  46. Lisouza FA, Owuor OP, Lalah JO. Variation in indoor levels of polycyclic aromatic hydrocarbons from burning various biomass types in the traditional grass-roofed households in Western Kenya. Environ Pollut. 2011;159:1810–5.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Institutes of Health (No. 1R21ES025032-01A1, S10 RR026437 and P30 DA012393). We thank Kristina Bello and Lawrence Chan for performing the analytical chemistry. We are very grateful to Gilberto Davila, Eduardo Canuz, Maritza Barrios, Expedita Ramirez, Micaela Marroquin and study participants in Guatemala.

Author information

Authors and Affiliations

  1. School of Nursing, University of California, San Francisco, San Francisco, CA, USA

    John R. Weinstein & Lisa M. Thompson

  2. School of Medicine, Boston University, Boston, MA, USA

    John R. Weinstein

  3. Centro de Estudios en Salud, Universidad del Valle, Guatemala City, Guatemala

    Anaité Diaz-Artiga

  4. Division of Clinical Pharmacology, Departments of Medicine and Bioengineering & Therapeutic Sciences, University of California San Francisco, San Francisco, CA, USA

    Neal Benowitz

  5. Nell Hodgson Woodruff School of Nursing, Emory University, Atlanta, GA, USA

    Lisa M. Thompson

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Correspondence to Lisa M. Thompson.

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Ethical approval

The study received ethical approval from the Committee for Human Research at UCSF and UVG and was registered on clinicaltrials.gov (ID: NCT02812914). Participants were informed of the study by trained field workers fluent in both Spanish and Mam.

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Weinstein, J.R., Diaz-Artiga, A., Benowitz, N. et al. Reductions in urinary metabolites of exposure to household air pollution in pregnant, rural Guatemalan women provided liquefied petroleum gas stoves. J Expo Sci Environ Epidemiol 30, 362–373 (2020). https://doi.org/10.1038/s41370-019-0163-0

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