Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Pesticide exposure and asthma morbidity in children residing in urban, multi-family housing

Journal of Exposure Science & Environmental Epidemiology (2023)Cite this article

Abstract

Background

Children are potentially more susceptible to the adverse effects of pesticides due to more sensitive organ systems and lower capacity to metabolize and eliminate chemicals compared to adults. The health risks are particularly concerning children with asthma, living in low-income neighborhoods in multi-family housing because of their impaired respiratory health, and factors associated with low-income, multi-family environments.

Objective

To assess the association between pesticide exposure and asthma morbidity among children 7–12 years residing in low-income, multi-family housing.

Methods

The concentrations of seven urinary pesticide biomarkers: 3,5,6-trichloro-2-pyridinol (TCPy), 2-isopropyl-4-methyl-6-hydroxypyrimidine, para-nitrophenol (PNP), 3-phenoxybenzoic acid (3-PBA), 4-fluoro-3-phenoxybenzoic acid, trans-3-(2,2-dichlorovinyl)-2,2-dimethyl-cyclopropane-1-carboxylic acid, and 2,4-dichlorophenoxyacetic acid (2,4-D) were measured. Children (n = 162) were followed for one year with three measures of pesticides biomarkers. Associations between individual biomarkers and asthma attack, asthma related health care utilization, and fraction of exhaled nitric oxide (FeNO), adjusting for demographic and household factors were examined with Generalized Estimating Equations (GEE). Weighted Quantile Sum (WQS) regression was used to examine the effect of pesticide mixture on asthma attacks and asthma-related health care utilization (HCU).

Results

In adjusted GEE models, positive non-significant associations were found between PNP and HCU (adjusted Odds Ratio(aOR):2.05 95% CI:0.76–5.52) and null associations for 3-PBA and HCU (aOR:1.07 95% CI: 0.88–1.29). Higher concentrations of PNP and 2,4-D were associated with significantly lower FeNO levels (PNP: −17.4%; 2,4-D:−19.74%). The mixture was positively associated with HCU in unadjusted (OR: 1.56 97.5% CI: 1.08–2.27) but not significant in adjusted models (aOR: 1.40 97.5% CI: .86–2.29). The non-specific pyrethroid biomarker 3-PBA at baseline contributed the greatest weight to the index (45%).

Significance

There were non-significant associations between pesticide biomarkers and respiratory outcomes in children with asthma. There was a suggestive association between urinary pesticide biomarkers and HCU. Further studies with larger sample sizes could help to confirm these findings.

Impact statement

  • Pesticide exposure among children in the urban environment is ubiquitous and there is a dearth of information on the impact of low-level chronic exposure in vulnerable populations. This study suggested that pesticide exposure at concentrations below the national average may not affect asthma morbidity in children. However, different biomarkers of pesticides showed different effects, but the mixture suggested increasing pesticide exposure results in asthma related HCU. The results may show that children with asthma may be at risk for negative health outcomes due to pesticides and the need to further examine this relationship.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Mean, median, interquartile range, 10th and 90th percentiles of pesticide biomarker concentrations (µg/g creatinine) by visit.
Fig. 2: Spearman correlations between pesticide biomarkers at each time point.

Data availability

Individuals who would like to access data can contact Dr. Werthmann (dwerthma@tulane.edu) with a specific request for data access.

References

  1. Akinbami LJ, Simon AE, Rossen LM. Changing trends in asthma prevalence among children. Pediatrics. 2016;137:1–7.

    Article  PubMed  Google Scholar 

  2. Guarnieri M, Balmes JR. Outdoor air pollution and asthma. Lancet. 2014;383:1581–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Snowden JM, Mortimer KM, Kang Dufour M-S, Tager IB. Population intervention models to estimate ambient NO2 health effects in children with asthma. J Expo Sci Environ Epidemiol. 2015;25:567–73.

    Article  CAS  PubMed  Google Scholar 

  4. Ye M, Beach J, Martin JW, Senthilselvan A. Pesticide exposures and respiratory health in general populations. J Environ Sci. 2017;51:361–70.

    Article  CAS  Google Scholar 

  5. Raanan R, Balmes JR, Harley KG, Gunier RB, Magzamen S, Bradman A, et al. Decreased lung function in 7-year-old children with early-life organophosphate exposure. Thorax. 2016;71:148–53.

    Article  PubMed  Google Scholar 

  6. Kim K-H, Kabir E, Jahan SA. Exposure to pesticides and the associated human health effects. Sci total Environ. 2017;575:525–35.

    Article  CAS  PubMed  Google Scholar 

  7. van Maele-Fabry G, Gamet-Payrastre L, Lison D. Residential exposure to pesticides as risk factor for childhood and young adult brain tumors: a systematic review and meta-analysis. Environ Int. 2017;106:69–90.

    Article  PubMed  Google Scholar 

  8. Blair A, Ritz B, Wesseling C, Freeman LB. Pesticides and human health. Occup Environ Med. 2015;72:81–82.

    Article  PubMed  Google Scholar 

  9. Mamane A, Raherison C, Tessier J-F, Baldi I, Bouvier G. Environmental exposure to pesticides and respiratory health. Eur Respi Rev. 2015;24:462–73.

    Article  Google Scholar 

  10. Patino EDL, Siegel JA. Indoor environmental quality in social housing: a literature review. Build Environ. 2018;131:231–41.

    Article  Google Scholar 

  11. Levy JI, Quirós-Alcalá L, Fabian MP, Basra K, Hansel NN. Established and emerging environmental contributors to disparities in asthma and chronic obstructive pulmonary disease. Curr Epidemiol Rep. 2018;5:114–24.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Martín Reina J, Duarte JA, Cerrillos L, Bautista Palomas JD, Moreno, Navarro IM. Insecticide reproductive toxicity profile: organophosphate, carbamate and pyrethroids. J Toxin. 2017;4:1–7.

    Google Scholar 

  13. Alavanja MCR, Bonner MR. Occupational pesticide exposures and cancer risk: a review. J Toxicol Environ Health, Part B. 2012;15:238–63.

    Article  CAS  Google Scholar 

  14. Rehman H, Aziz A-T, Saggu S, Abbas ZK, Mohan A, Ansari AA. Systematic review on pyrethroid toxicity with special reference to deltamethrin. J Entomol Zool Stud. 2014;2:60–70.

    Google Scholar 

  15. Chen M, Chang C-H, Tao L, Lu C. Residential exposure to pesticide during childhood and childhood cancers: a meta-analysis. Pediatrics. 2015;136:719–29.

    Article  PubMed  Google Scholar 

  16. Saillenfait A-M, Ndiaye D, Sabaté J-P. Pyrethroids: exposure and health effects–an update. Int J Hyg Environ Health. 2015;218:281–92.

    Article  CAS  PubMed  Google Scholar 

  17. Mink PJ, Mandel JS, Sceurman BK, Lundin JI. Epidemiologic studies of glyphosate and cancer: a review. Regul Toxicol Pharmacol. 2012;63:440–52.

    Article  CAS  PubMed  Google Scholar 

  18. Koureas M, Tsakalof A, Tsatsakis A, Hadjichristodoulou C. Systematic review of biomonitoring studies to determine the association between exposure to organophosphorus and pyrethroid insecticides and human health outcomes. Toxicol Lett. 2012;210:155–68.

    Article  CAS  PubMed  Google Scholar 

  19. Li AJ, Kannan K. Urinary concentrations and profiles of organophosphate and pyrethroid pesticide metabolites and phenoxyacid herbicides in populations in eight countries. Environ Int. 2018;121:1148–54.

    Article  CAS  PubMed  Google Scholar 

  20. Stanfield Z, Setzer RW, Hull V, Sayre RR, Isaacs KK, Wambaugh JF. Bayesian inference of chemical exposures from NHANES urine biomonitoring data. J Expo Sci Environ Epidemiol. 2022;32:1–14.

  21. Barr DB. Biomonitoring of exposure to pesticides. J Chem Health Saf. 2008;15:20–29.

    Article  CAS  Google Scholar 

  22. Zhang Y, Dong T, Hu W, Wang X, Xu B, Lin Z, et al. Association between exposure to a mixture of phenols, pesticides, and phthalates and obesity: comparison of three statistical models. Environ Int. 2019;123:325–36.

    Article  CAS  PubMed  Google Scholar 

  23. Li W, Xiao H, Wu H, Xu X, Zhang Y. Organophosphate pesticide exposure and biomarkers of liver injury/liver function. Liver Int. 2022;42:2713–23.

    Article  CAS  PubMed  Google Scholar 

  24. Xu H, Mao Y, Xu B. Association between pyrethroid pesticide exposure and hearing loss in adolescents. Environ Res. 2020;187:109640.

    Article  CAS  PubMed  Google Scholar 

  25. Pohl HR, McClure P, Anatra-Cordone M. Mixtures of insecticides: pyrethroids, organophosphorus compounds, and carbamates. Agency for Toxic Substances and Disease Registry US Department of Health and Human Services Public Health Service. 2018.

  26. Hu P, Su W, Vinturache A, Gu H, Cai C, Lu M, et al. Urinary 3-phenoxybenzoic acid (3-PBA) concentration and pulmonary function in children: A National Health and Nutrition Examination Survey (NHANES) 2007–12 analysis. Environ Pollut. 2021;270:116178.

    Article  CAS  PubMed  Google Scholar 

  27. Saillenfait A-M, Malard S. Human risk associated with long-term exposure to pyrethroid insecticides. Pyrethroid Insecticides. 2020;92:259–303.

  28. Burns CJ, Swaen GMH. Review of 2, 4-dichlorophenoxyacetic acid (2, 4-D) biomonitoring and epidemiology. Crit Rev Toxicol. 2012;42:768–86.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Perry J, Cotton J, Rahman MA, Brumby SA. Organophosphate exposure and the chronic effects on farmers: a narrative review. Rural Remote Health. 2020;20:4508.

    PubMed  Google Scholar 

  30. Kumar V, Kumar P. Pesticides in agriculture and environment: impacts on human health. Contam Agric Environ: Health Risks Remediat. 2019;1:76–95.

    Google Scholar 

  31. Davis MD, Wade EL, Restrepo PR, Roman-Esteva W, Bravo R, Kuklenyik P, et al. Semi-automated solid phase extraction method for the mass spectrometric quantification of 12 specific metabolites of organophosphorus pesticides, synthetic pyrethroids, and select herbicides in human urine. J Chromatogr B. 2013;929:18–26.

    Article  CAS  Google Scholar 

  32. Prevention C for DC and. NHANES laboratory/medical technologists procedures manual. Atlanta, GA: Centers for Disease Control and Prevention 2001.

  33. Dweik RA, Boggs PB, Erzurum SC, Irvin CG, Leigh MW, Lundberg JO, et al. An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med. 2011;184:602–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Matt GE, Wahlgren DR, Hovell MF, Zakarian JM, Bernert JT, Meltzer SB, et al. Measuring environmental tobacco smoke exposure in infants and young children through urine cotinine and memory-based parental reports: empirical findings and discussion. Tob Control. 1999;8:282–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Coombs KC, Chew GL, Schaffer C, Ryan PH, Brokamp C, Grinshpun SA, et al. Indoor air quality in green-renovated vs. non-green low-income homes of children living in a temperate region of US (Ohio). Sci Total Environ. 2016;554:178–85.

    Article  PubMed  Google Scholar 

  36. Greenland S, Pearce N. Statistical foundations for model-based adjustments. Annu Rev Public Health. 2015;36:89–108.

    Article  PubMed  Google Scholar 

  37. Barr DB, Landsittel D, Nishioka M, Thomas K, Curwin B, Raymer J, et al. A survey of laboratory and statistical issues related to farmworker exposure studies. Environ Health Perspect. 2006;114:961–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Levin-Schwartz Y, Gennings C, Schnaas L, del Carmen Hernández Chávez M, Bellinger DC, Téllez-Rojo MM, et al. Time-varying associations between prenatal metal mixtures and rapid visual processing in children. Environ Health. 2019;18:1–12.

    Article  CAS  Google Scholar 

  39. Carrico C, Gennings C, Wheeler DC, Factor-Litvak P. Characterization of weighted quantile sum regression for highly correlated data in a risk analysis setting. J Agric Biol Environ Stat. 2015;20:100–20.

    Article  PubMed  Google Scholar 

  40. Buralli RJ, Dultra AF, Ribeiro H. Respiratory and allergic effects in children exposed to pesticides—a systematic review. Int J Environ Res Public Health. 2020;17:2740.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Perla ME, Rue T, Cheadle A, Krieger J, Karr CJ. Biomarkers of insecticide exposure and asthma in children: a National Health and Nutrition Examination Survey (NHANES) 1999–2008 analysis. Arch Environ Occup Health. 2015;70:309–22.

    Article  CAS  PubMed  Google Scholar 

  42. Salameh PR, Baldi I, Brochard P, Raherison C, Abi Saleh B, Salamon R. Respiratory symptoms in children and exposure to pesticides. Eur Respir J. 2003;22:507–12.

    Article  CAS  PubMed  Google Scholar 

  43. Salam MT, Li Y-F, Langholz B, Gilliland FD, Study CH. Early-life environmental risk factors for asthma: findings from the Children’s Health Study. Environ Health Perspect. 2004;112:760–5.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Adamkiewicz G, Zota AR, Fabian MP, Chahine T, Julien R, Spengler JD, et al. Moving environmental justice indoors: understanding structural influences on residential exposure patterns in low-income communities. Am J Public Health. 2011;101:S238–S245.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Lu C, Adamkiewicz G, Attfield KR, Kapp M, Spengler JD, Tao L, et al. Household pesticide contamination from indoor pest control applications in urban low-income public housing dwellings: a community-based participatory research. Environ Sci Technol. 2013;47:2018–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Chapman GM, Bravo R, Stanelle RD, Watson CH, Valentín-Blasini L. Sensitive and selective gas chromatography-tandem mass spectrometry method for the detection of nitrobenzene in tobacco smoke. J Chromatogr A. 2018;1565:124–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Malinovschi A, Backer V, Harving H, Porsbjerg C. The value of exhaled nitric oxide to identify asthma in smoking patients with asthma-like symptoms. Respir Med. 2012;106:794–801.

    Article  PubMed  Google Scholar 

  48. O’Brien KM, Upson K, Cook NR, Weinberg CR. Environmental chemicals in urine and blood: improving methods for creatinine and lipid adjustment. Environ Health Perspect. 2016;124:220–7.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the children and their parents for their participation and our community partners for their assistance throughout the study. We also thank Mark Davis and William Roman for the measurement of the pesticide biomarkers and Connie Sosnoff for the measurement of cotinine.

Funding

This study was funded by the Centers for Disease Control and Prevention (CDC) grant #5UO1EH000990 with supplemental funding from the U.S. Environmental Protection Agency (EPA) interagency agreement #DW-75–9584500 and the U.S. Department of Housing and Urban Development (HUD) interagency agreement # I-PHI-01062.

Author information

Authors and Affiliations

  1. Tulane University, School of Public Health and Tropical Medicine, New Orleans, LA, USA

    Derek W. Werthmann & Felicia A. Rabito

  2. Harvard, T.H. Chan School of Public Health, Boston, MA, USA

    Gary Adamkiewicz

  3. University of Cincinnati, Department of Environmental and Public Health Sciences, Cincinnati, OH, USA

    Tiina Reponen

  4. Division of Laboratory Sciences, National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA, USA

    Antonia M. Calafat & Maria Ospina

  5. Division of Environmental Health Science and Practice, National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA, USA

    Ginger L. Chew

Authors
  1. Derek W. Werthmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Felicia A. Rabito
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gary Adamkiewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tiina Reponen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Antonia M. Calafat
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maria Ospina
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ginger L. Chew
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DW had full access to the data and takes responsibility for the integrity of the data and accuracy of analysis; DW, FR, GC, AC, MO were involved in the design and conduct of the analysis; DW, FR, GA, TR, AC, MO, GC contributed to the drafting of the manuscript; DW, FR, GA, TR, AC, MO, GC were involved in the editing of the manuscript. All authors approved the manuscript for submission.

Corresponding author

Correspondence to Derek W. Werthmann.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Werthmann, D.W., Rabito, F.A., Adamkiewicz, G. et al. Pesticide exposure and asthma morbidity in children residing in urban, multi-family housing. J Expo Sci Environ Epidemiol (2023). https://doi.org/10.1038/s41370-023-00524-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41370-023-00524-2

Keywords

  • Pesticides
  • Asthma
  • Pyrethroids
  • Organophosphorous
  • 2
  • 4-D

Search

Advanced search

Quick links