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.

  • Article
  • Published:

Neurobehavioral performance of dual exposure to organophosphate pesticides and PAHs among farmers in rural agriculture communities

Journal of Exposure Science & Environmental Epidemiology volume 36, pages 343–354 (2026)Cite this article

Abstract

Background

Farmers in Northern Thailand are chronically exposed to organophosphate pesticides (OPs) through agricultural activities and to polycyclic aromatic hydrocarbons (PAHs) from seasonal biomass burning. Both toxicants have been linked to neurobehavioral impairments, but little is known about their combined effects.

Objectives

This study aimed to investigate the association between urinary biomarkers of exposure to OPs and PAHs and neurobehavioral performance among farmers in rural agricultural communities, including potential interaction effects of co-exposure.

Methods

A total of 115 farmers aged 20–70 years in Northern Thailand were recruited. Urinary dialkyl phosphate (DAP) metabolites, biomarkers of OPs exposure, and 1-hydroxypyrene (1-OHP), a biomarker of PAHs exposure, were measured. Neurobehavioral performance was assessed using the digit span test (DST), Purdue pegboard test (PEG), and visual-motor integration (VMI) test.

Results

Higher urinary dimethylphosphate (DMP) levels were significantly associated with lower DST forward digit span (β ± SE = −0.807 ± 0.284) and maximum forward digit span scores (β ± SE = −0.350 ± 0.159), indicating cognitive impairment. Increased 1-OHP levels were significantly correlated with lower VMI raw (β ± SE = −0.529 ± 0.236) and standard scores (β ± SE = −3.188 ± 1.239), suggesting impaired visual-motor integration. Notably, significant interaction effects were observed between DMP and 1-OHP on forward digit span (β ± SE = −0.244 ± 0.104) and VMI raw scores (β ± SE = −0.311 ± 0.121), and between DEP and 1-OHP on VMI performance (β ± SE = −0.264 ± 0.131 for raw score and −1.755 ± 0.686 for standard score), indicating that co-exposure may amplify neurobehavioral deficits.

Impact

  • This study underscores the need for integrated interventions through improved pesticide safety, consistent use of personal protective equipment, and air pollution mitigation strategies.

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

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Data will be made available on request.

References

  1. Khode D, Hepat A, Mudey A, Joshi A. Health-related challenges and programs among agriculture workers: a narrative review. Cureus. 2024;16:e57222. https://doi.org/10.7759/cureus.57222.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Clarke K, Manrique A, Sabo-Attwood T, Coker ES. A narrative review of occupational air pollution and respiratory health in farmworkers. Int J Environ Res Public Health. 2021;18:4097. https://doi.org/10.3390/ijerph18084097.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Forté CA, Colacino J, Polemi K, Guytingco A, Peraino NJ, Jindaphong S, et al. Pesticide exposure and adverse health effects associated with farmwork in Northern Thailand. J Occup Health. 2021;63:e12222. https://doi.org/10.1002/1348-9585.12222.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Moran J, NaSuwan C, Poocharoen OO. The haze problem in Northern Thailand and policies to combat it: a review. Environ Sci Policy. 2019;97:1–15. https://doi.org/10.1016/j.envsci.2019.03.016.

    Article  Google Scholar 

  5. Office of Agriculture Regulation, Department of Agriculture. Statistics of imported hazardous chemicals into Thailand. 2024. Retrieved 10 December 2024, from https://www.doa.go.th/ard/?page_id=386.

  6. Inlaung K, Chotamonsak C, Macatangay R, Surapipith V. Assessment of transboundary PM₂.₅ from biomass burning in Northern Thailand using the WRF-Chem model. Toxics. 2024;12:462. https://doi.org/10.3390/toxics12070462.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Ayeni EA, Aldossary AM, Ayejoto DA, Gbadegesin LA, Alshehri AA, Alfassam HA, et al. Neurodegenerative diseases: implications of environmental and climatic influences on neurotransmitters and neuronal hormones activities. Int J Environ Res Public Health. 2022;19:12495. https://doi.org/10.3390/ijerph191912495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kamel F, Hoppin JA. Association of pesticide exposure with neurologic dysfunction and disease. Environ Health Perspect. 2004;112:950–8. https://doi.org/10.1289/ehp.7135.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Liu X, Huang J, Song C, Zhang T, Liu Y, Yu L. Neurodevelopmental toxicity induced by PM₂.₅ exposure and its possible role in neurodegenerative and mental disorders. Hum Exp Toxicol. 2023;42. https://doi.org/10.1177/09603271231191436.

  10. Tsai YH, Lein PJ. Mechanisms of organophosphate neurotoxicity. Curr Opin Toxicol. 2021;26:49–60. https://doi.org/10.1016/j.cotox.2021.04.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Jaiswal C, Singh AK. Particulate matter exposure and its consequences on hippocampal neurogenesis and cognitive function in experimental models. Environ Pollut. 2024;363:125275. https://doi.org/10.1016/j.envpol.2024.125275.

    Article  CAS  PubMed  Google Scholar 

  12. Humphreys J, Valdés Hernández MDC. Impact of polycyclic aromatic hydrocarbon exposure on cognitive function and neurodegeneration in humans: a systematic review and meta-analysis. Front Neurol. 2023;13:1052333. https://doi.org/10.3389/fneur.2022.1052333.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Alter NC, Whitman EM, Bellinger DC, Landrigan PJ. Quantifying the association between PM2.5 air pollution and IQ loss in children: a systematic review and meta-analysis. Environ Health. 2024;23:101. https://doi.org/10.1186/s12940-024-01122-x.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Amnuaylojaroen T, Parasin N. Pathogenesis of PM₂.₅-related disorders in different age groups: children, adults, and the elderly. Epigenomes. 2024;8:13. https://doi.org/10.3390/epigenomes8020013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Thammachai A, Suwannakul B, Sangkarit N, Hongsibsong S, Rohitrattana J, Sapbamrer R. Neurobehavioral performance in preschool children exposed postnatally to organophosphates in agricultural regions, Northern Thailand. Toxics. 2024;12:855. https://doi.org/10.3390/toxics12120855.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Sapbamrer P, Assavanopakun P, Panumasvivat J. Decadal trends in ambient air pollutants and their association with COPD and lung cancer in Upper Northern Thailand: 2013–2022. Toxics. 2024;12:321. https://doi.org/10.3390/toxics12050321.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Prapamontol T, Sutan K, Laoyang S, Hongsibsong S, Lee G, Yano Y, et al. Cross-validation of gas chromatography-flame photometric detection and gas chromatography-mass spectrometry methods for measuring dialkylphosphate metabolites of organophosphate pesticides in human urine. Int J Hyg Environ Health. 2014;217:554–66.

    Article  CAS  PubMed  Google Scholar 

  18. Hornung RW, Reed LD. Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg. 1990;5:46–51.

    Article  CAS  Google Scholar 

  19. Chetiyanukornkul T, Toriba A, Kameda T, Tang N, Hayakawa K. Simultaneous determination of urinary hydroxylated metabolites of naphthalene, fluorene, phenanthrene, fluoranthene, and pyrene as multiple biomarkers of exposure to polycyclic aromatic hydrocarbons. Anal Bioanal Chem. 2006;386:712–8. https://doi.org/10.1007/s00216-006-0628-6.

    Article  CAS  PubMed  Google Scholar 

  20. Sutan K, Naksen W, Prapamontol T. A simple high-performance liquid chromatography coupled to fluorescence detection method using column-switching technique for measuring urinary 1-hydroxypyrene from environmental exposure. Chiang Mai J Sci. 2017;44:1441–52.

    CAS  Google Scholar 

  21. Rohlman DS, Lucchini R, Anger WK, Bellinger DC, van Thriel C. Neurobehavioral testing in human risk assessment. Neurotoxicology. 2008;29:556–67.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Rohitrattana J, Siriwong W, Suittiwan P, Robson MG, Strickland PO, Rohlman DS, et al. Adaptation of a neurobehavioral test battery for Thai children. Rocz Panstw Zakl Hig. 2014;65:205–12.

    PubMed  PubMed Central  Google Scholar 

  23. Thammachai A, Sapbamrer R, Rohitrattana J, Tongprasert S, Hongsibsong S, Wangsan K. The reliability of neurobehavioral tests in a Thai adult population. Dement Neuropsychol. 2022;16:324–31. https://doi.org/10.1590/1980-5764-DN-2021-0115.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Beery KE, Buktenica NA, Beery NA. The Beery–Buktenica developmental test of Visual-Motor Integration: administration, scoring, and teaching manual. 6th ed. Pearson; 2010.

  25. Spencer TD, Kruse L. Beery-Buktenica developmental test of visual-motor integration. In: Volkmar FR, editor. Encyclopedia of autism spectrum disorders. USA: Springer; 2013. pp 400–4.

  26. Kaushal J, Khatri M, Arya SK. A treatise on organophosphate pesticide pollution: current strategies and advancements in their environmental degradation and elimination. Ecotoxicol Environ Saf. 2021;207:111483. https://doi.org/10.1016/j.ecoenv.2020.111483.

    Article  CAS  PubMed  Google Scholar 

  27. Chittrakul J, Sapbamrer R, Hongsibsong S. Exposure to organophosphate insecticides, inappropriate personal protective equipment use, and cognitive performance among pesticide applicators. Front Public Health. 2022;10:1060284. https://doi.org/10.3389/fpubh.2022.1060284.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Ore OT, Adeola AO, Bayode AA, Adedipe DT, Nomngongo PN. Organophosphate pesticide residues in environmental and biological matrices: occurrence, distribution and potential remedial approaches. Environ Chem Ecotoxicol. 2023;5:9–23. https://doi.org/10.1016/j.enceco.2022.10.004.

    Article  CAS  Google Scholar 

  29. Staudacher P, Fuhrimann S, Farnham A, Mora AM, Atuhaire A, Niwagaba C, et al. Comparative analysis of pesticide use determinants among smallholder farmers from Costa Rica and Uganda. Environ Health Insights. 2020;14:1178630220972417. https://doi.org/10.1177/1178630220972417.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ragnarsdottir KV. Environmental fate and toxicology of organophosphate pesticides. J Geol Soc. 2000;157:859–76. https://doi.org/10.1144/jgs.157.6.859.

    Article  CAS  Google Scholar 

  31. Gorbounov M, Halloran P, Masoudi Soltani S. Hydrophobic and hydrophilic functional groups and their impact on physical adsorption of CO₂ in the presence of H₂O: a critical review. J CO₂ Util. 2024;86:102908. https://doi.org/10.1016/j.jcou.2024.102908.

    Article  CAS  Google Scholar 

  32. PubChem, National Library of Medicine. Explore chemistry. 2025. Retrieved 2 December 2024, from https://pubchem.ncbi.nlm.nih.gov/.

  33. Paluang P, Thavorntam W, Phairuang W. The spatial–temporal emission of air pollutants from biomass burning during haze episodes in Northern Thailand. Fire. 2024;7:122. https://doi.org/10.3390/fire7040122.

    Article  Google Scholar 

  34. Mallisuwan S, Yooyen S, Pimnoo A, Delmaire C. Monitoring hotspots using thermal sensors on MODIS Aqua/Terra satellite system: a case study of national park areas in Northern Thailand. Adv Remote Sens. 2023;12:47–69. https://doi.org/10.4236/ars.2023.122003.

    Article  Google Scholar 

  35. Zheng H, Qu C, Zhang J, Talpur SA, Ding Y, Xing X, et al. Polycyclic aromatic hydrocarbons (PAHs) in agricultural soils from Ningde, China: levels, sources, and human health risk assessment. Environ Geochem Health. 2019;41:907–19. https://doi.org/10.1007/s10653-018-0188-7.

    Article  CAS  PubMed  Google Scholar 

  36. Nakhjirgan P, Kashani H, Kermani M. Exposure to outdoor particulate matter and risk of respiratory diseases: a systematic review and meta-analysis. Environ Geochem Health. 2023;46:20. https://doi.org/10.1007/s10653-023-01807-1.

    Article  CAS  PubMed  Google Scholar 

  37. Strobl K, Irfan SA, Masood H, Latif N, Kurmi O. Association between PM₁₀ exposure and risk of myocardial infarction in adults: a systematic review and meta-analysis. PLoS ONE. 2024;19:e0301374. https://doi.org/10.1371/journal.pone.0301374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Sapbamrer R, Thammachai A. Factors affecting use of personal protective equipment and pesticide safety practices: a systematic review. Environ Res. 2020;185:109444. https://doi.org/10.1016/j.envres.2020.109444.

    Article  CAS  PubMed  Google Scholar 

  39. Suratman S, Edwards JW, Babina K. Organophosphate pesticides exposure among farmworkers: pathways and risk of adverse health effects. Rev Environ Health. 2015;30:65–79. https://doi.org/10.1515/reveh-2014-0072.

    Article  CAS  PubMed  Google Scholar 

  40. Akinrinade OE, Rosa AH. Current level, sources, and risk of human exposure to PAHs, PBDEs, and PCBs in South American outdoor air: a critical review. Environ Res. 2025. https://doi.org/10.1016/j.envres.2025.120941.

  41. Pinakana SD, Garcia Patlan C, Mendez E, Raysoni AU. A pilot study on particulate matter concentrations from cooking and its effects on indoor air pollution in a Mexican American household in Mission, South Texas, USA. Case Stud Chem Environ Eng. 2024;9:100757. https://doi.org/10.1016/j.cscee.2024.100757.

    Article  CAS  Google Scholar 

  42. Amnuaylojaroen T, Parasin N. Perspective on particulate matter: from biomass burning to the health crisis in mainland Southeast Asia. Toxics. 2023;11:553. https://doi.org/10.3390/toxics11070553.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Song W, Zhang YL, Zhang Y, Cao F, Rauber M, Salazar G, et al. Is biomass burning always a dominant contributor of fine aerosols in Upper Northern Thailand? Environ Int. 2022;168:107466. https://doi.org/10.1016/j.envint.2022.107466.

    Article  CAS  PubMed  Google Scholar 

  44. Pongpiachan S, Hattayanone M. Effect of agricultural waste burning season on PM₂.₅-bound polycyclic aromatic hydrocarbon (PAH) levels in Northern Thailand. Atmos Pollut Res. 2017;8:1069–80. https://doi.org/10.1016/j.apr.2017.04.009.

    Article  Google Scholar 

  45. Woods DL, Kishiyama MM, Lund EW, Herron TJ, Edwards B, Poliva O, et al. Improving digit span assessment of short-term verbal memory. J Clin Exp Neuropsychol. 2011;33:101–11. https://doi.org/10.1080/13803395.2010.493149.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Budson AE, Price BH. Memory dysfunction. N Engl J Med. 2005;352:692–9. https://doi.org/10.1056/NEJMra041071.

    Article  CAS  PubMed  Google Scholar 

  47. Chen Y. Organophosphate-induced brain damage: mechanisms, neuropsychiatric and neurological consequences, and potential therapeutic strategies. Neurotoxicology. 2012;33:391–400. https://doi.org/10.1016/j.neuro.2012.03.011.

    Article  CAS  PubMed  Google Scholar 

  48. Torres-Altoro MI, Mathur BN, Drerup JM, Thomas R, Lovinger DM, O’Callaghan JP, et al. Organophosphates dysregulate dopamine signaling, glutamatergic neurotransmission, and induce neuronal injury markers in striatum. J Neurochem. 2011;119:303–13. https://doi.org/10.1111/j.1471-4159.2011.07428.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Pearson JN, Patel M. The role of oxidative stress in organophosphate and nerve agent toxicity. Ann N Y Acad Sci. 2016;1378:17–24. https://doi.org/10.1111/nyas.13115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Voorhees JR, Remy MT, Erickson CM, Dutca LM, Brat DJ, Pieper AA. Occupational-like organophosphate exposure disrupts microglia and accelerates deficits in a rat model of Alzheimer’s disease. npj Aging Mech Dis. 2019;5:3. https://doi.org/10.1038/s41514-018-0033-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Singh S. Organophosphorous poisoning: an evidence-based approach. Med J Armed Forces India. 2004;60:2–4.

    Article  PubMed  Google Scholar 

  52. Miall RC, Reckess GZ, Imamizu H. The cerebellum coordinates eye and hand tracking movements. Nat Neurosci. 2001;4:638–44. https://doi.org/10.1038/88465.

    Article  CAS  PubMed  Google Scholar 

  53. Battaglia-Mayer A, Caminiti R. Parieto-frontal networks for eye-hand coordination and movements. Handb Clin Neurol. 2018;151:499–524. https://doi.org/10.1016/B978-0-444-63622-5.00026-7.

    Article  PubMed  Google Scholar 

  54. Peterson BS, Rauh VA, Bansal R, Hao X, Toth Z, Nati G, et al. Effects of prenatal exposure to air pollutants on brain white matter, cognition, and behavior in later childhood. JAMA Psychiatry. 2015;72:531–40. https://doi.org/10.1001/jamapsychiatry.2015.57.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The Authors would like to thank the staff of Community Health Promotion Hospitals in Phayao province for their cooperation. We would like to acknowledge the assistance of ChatGPT for improving English during the preparation of this manuscript.

Funding

The authors would like to acknowledge the financial support provided by CMU Mid-Career Research Fellowship Program, Chiang Mai University, Grant number MRCMU2566R_007 and MRCMUR2567-2_007.

Author information

Authors and Affiliations

  1. Department of Physical Therapy, School of Allied Health Sciences, University of Phayao, Phayao, Thailand

    Noppharath Sangkarit, Ajchamon Thammachai & Boonsita Suwannakul

  2. School of Health Sciences Research, Research Institute for Health Sciences, Chiang Mai University, Chiang Mai, Thailand

    Surat Hongsibsong

  3. Center for Safety, Health and Environment of Chulalongkorn University, Bangkok, Thailand

    Juthasiri Rohitrattana

  4. Department of Community Medicine, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand

    Jinjuta Panumasvivat, Pheerasak Assavanopakun & Ratana Sapbamrer

  5. Environmental and Occupational Medicine Excellence Center (EnOMEC), Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand

    Jinjuta Panumasvivat, Pheerasak Assavanopakun & Ratana Sapbamrer

Authors
  1. Noppharath Sangkarit
    View author publications

    Search author on:PubMed Google Scholar

  2. Ajchamon Thammachai
    View author publications

    Search author on:PubMed Google Scholar

  3. Boonsita Suwannakul
    View author publications

    Search author on:PubMed Google Scholar

  4. Surat Hongsibsong
    View author publications

    Search author on:PubMed Google Scholar

  5. Juthasiri Rohitrattana
    View author publications

    Search author on:PubMed Google Scholar

  6. Jinjuta Panumasvivat
    View author publications

    Search author on:PubMed Google Scholar

  7. Pheerasak Assavanopakun
    View author publications

    Search author on:PubMed Google Scholar

  8. Ratana Sapbamrer
    View author publications

    Search author on:PubMed Google Scholar

Contributions

Ratana Sapbamrer: conceptualization, project administration, supervision, funding acquisition, methodology, validation, investigation, formal analysis, data curation, resource, visualization, writing-original draft, writing-review and editing. Noppharath Sangkarit: Conceptualization, Methodology, Validation, Investigation, Formal analysis, Visualization, Data curation, Writing-original draft. Boonsita Suwannakul: conceptualization, methodology, validation, investigation, formal analysis, visualization, data curation, writing-original draft. Ajchamon Thammachai: conceptualization, methodology, validation, investigation, formal analysis, visualization, data curation, writing-original draft. Surat Hongsibsong: validation, investigation, formal analysis. Juthasiri Rohitrattana: validation, methodology. Jinjuta Panumasvivat: validation, methodology. Pheerasak Assavanopakun: validation, methodology.

Corresponding author

Correspondence to Ratana Sapbamrer.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethical approval and consent to participate

This study was conducted in strict accordance with the ethical standards established by the Research Ethics Committee of the Faculty of Medicine, Chiang Mai University, Thailand (Approval No. 307/2023, date of approval 25 August 2023). Informed written consent was obtained from all participants during the first visit and all methods were performed in accordance with the relevant guidelines and regulations.

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

Sangkarit, N., Thammachai, A., Suwannakul, B. et al. Neurobehavioral performance of dual exposure to organophosphate pesticides and PAHs among farmers in rural agriculture communities. J Expo Sci Environ Epidemiol 36, 343–354 (2026). https://doi.org/10.1038/s41370-025-00815-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Version of record:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41370-025-00815-w

Keyword

Search

Advanced search

Quick links