Skip to main content

Advertisement

SpringerLink
Log in

Association of immunotoxicological indices with lung cancer biomarkers in poultry, grape, and rose farming workers

  • Original Article
  • Published:
Toxicological Research Aims and scope Submit manuscript

Abstract

Exposure to occupational hazards like dust, pesticides, diesel emission particles, or physical hazards in the agricultural sector is known to cause adverse health effects on farm workers. Our study aimed at addressing the association of immunomodulatory status with plasma levels of lung cancer biomarkers in farming population, attempting to recognition of vulnerable farming group. Blood samples from apparently healthy 51 chicken husbandry, 19 grape orchard, and 21 rose greenhouse workers were subjected to evaluate plasma levels of two representative lung cancer biomarkers, pro-gastrin releasing peptide (Pro-GRP) and cytokeratin fragment 19 (CYFRA 21-1). Peripheral blood mononuclear cells obtained from farmers were used for natural killer (NK) cell phenotyping and cytokines (interferon-gamma, IFN-γ and interleukin-13, IL-13) profiling in the culture supernatant. Compared to the rose greenhouse farmers, the grape orchard and chicken husbandry workers revealed a significantly upregulated plasma Pro-GRP and CYFRA 21-1 level. A low proportion of NK cells was observed among the female grape orchard workers and a lowered IFN- γ:IL-13 ratio was seen in the grape and chicken husbandry workers than the rose workers. Our findings imply that grape orchard and chicken husbandry workers have more disturbed immune homeostasis implicated with augmentation in the levels of lung cancer biomarkers than the rose greenhouse workers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Raw data for tables and figures are not publicly available to preserve participants’ privacy under the regulation of Institutional Review Board of Daegu Catholic University. Data requests can be made to the Institutional Review Board of Daegu Catholic University via mail to: 13–13, Hayang-ro, Gyeongsan-Si, Gyeongbuk 38,430, Republic of Korea.

References

  1. International Labour Organization (2009) Agriculture: a hazardous work: occupational safety and health. http://www.ilo.org/safework/areasofwork/hazardous-work/WCMS_110188/lang--en/index.htm.

  2. White G, Cessna A (1989) Occupational hazards of farming. Can Fam Physician 35:2331–2336

    CAS  PubMed  PubMed Central  Google Scholar 

  3. International Labour Office (2011) Safety and health in agriculture. ILO Code of practice. https://www.ilo.org/wcmsp5/groups/public/---ed_dialogue/---sector/documents/normativein strument/wcms_161135.pdf.

  4. Shin SJ, Song ES, Kim JW, Lee JH et al (2019) Major environmental characteristics of swine husbandry that affect exposure to dust and airborne endotoxins. J Toxicol Environ Heal Part A 82:233–243. https://doi.org/10.1080/15287394.2019.1584596

    Article  CAS  Google Scholar 

  5. Roque K, Lim GD, Jo JH, Shin KM et al (2016) Epizootiological characteristics of viable bacteria and fungi in indoor air from porcine, chicken, or bovine husbandry confinement buildings. J Vet Sci 17:531–538. https://doi.org/10.4142/jvs.2016.17.4.531

    Article  PubMed  PubMed Central  Google Scholar 

  6. Gautam R, Heo Y, Lim GD, Song ES et al (2018) Altered immune responses in broiler chicken husbandry workers and their association with endotoxin exposure. Ind Health 56:10–19. https://doi.org/10.2486/indhealth.2017-0049

    Article  CAS  PubMed  Google Scholar 

  7. Moran RE, Bennett DH, Garcia J, Schenker MB (2014) Occupational exposure to particulate matter from three agricultural crops in California. Int J Hyg Environ Health 217:226–230. https://doi.org/10.1016/j.ijheh.2013.05.002

    Article  PubMed  Google Scholar 

  8. Arslan S, Aybek A, Ekerbiçer HÇ (2010) Measurement of personal PM10, PM2.5 and PM1 exposures in tractor and combine operations and evaluation of health disturbances of operators. J Agric Sci 16:104–115. https://doi.org/10.1501/Tarimbil_0000001127

    Article  Google Scholar 

  9. Sauvé JF, Stapleton EM, O’Shaughnessy PT et al (2020) Diesel exhaust exposure during farming activities: statistical modeling of continuous black carbon concentrations. Ann Work Expo Heal 64:503–513. https://doi.org/10.1093/annweh/wxaa032

    Article  CAS  Google Scholar 

  10. FAO (2021) Pesticides use. global, regional and country trends, 1990–2018. FAOSTAT analytical brief series No. 16. FAO, Rome (Italy), p 10. https://www.fao.org/documents/card/en?details=cb3411en%2f

  11. Nguyen THY, Bertin M, Bodin J, Fouquet N et al (2018) Multiple exposures and coexposures to occupational hazards among agricultural workers: a systematic review of observational studies. Saf Health Work 9:239–248. https://doi.org/10.1016/j.shaw.2018.04.002

    Article  PubMed  PubMed Central  Google Scholar 

  12. Lerro CC, Koutros S, Andreotti G, Sandler DP et al (2019) Cancer incidence in the agricultural health study after 20 years of follow-up. Cancer Causes Control 30:311–322. https://doi.org/10.1007/s10552-019-01140-y

    Article  PubMed  PubMed Central  Google Scholar 

  13. Nordgren TM, Charavaryamath C (2018) Agriculture occupational exposures and factors affecting health effects. Curr Allergy Asthma Rep 18:1–8. https://doi.org/10.1007/s11882-018-0820-8

    Article  Google Scholar 

  14. Piel C, Pouchieu C, Carles C, Béziat B et al (2019) Agricultural exposures to carbamate herbicides and fungicides and central nervous system tumour incidence in the cohort AGRICAN. Environ Int 130:1048. https://doi.org/10.1016/j.envint.2019.05.070

    Article  CAS  Google Scholar 

  15. Talibov M, Tual S, Morlais F, Meryet-Figuière M et al (2022) Colorectal cancer among farmers in the AGRICAN cohort study. Cancer Epidemiol 78:102125. https://doi.org/10.1016/j.canep.2022.102125

    Article  PubMed  Google Scholar 

  16. Candeias MS, Gaipl SU (2016) The immune system in cancer prevention, development and therapy. Anticancer Agents Med Chem 16:101–107. https://doi.org/10.2174/1871520615666150824153523

    Article  CAS  PubMed  Google Scholar 

  17. Fridman WH, Pagès F, Saut̀s-FridmanGalon CJ (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12:298–306. https://doi.org/10.1038/nrc3245

    Article  CAS  PubMed  Google Scholar 

  18. Balkwill FR, Capasso M, Hagemann T (2012) The tumor microenvironment at a glance. J Cell Sci 125:5591–5596. https://doi.org/10.1242/jcs.116392

    Article  CAS  PubMed  Google Scholar 

  19. Maharjan A, Gautam R, Jo JH, Acharya M et al (2022) Comparison of overall immunity levels among workers at grape orchard, rose greenhouse, and open-field onion farm. Saf Health Work 13:248–254. https://doi.org/10.1016/j.shaw.2021.12.002

    Article  PubMed  Google Scholar 

  20. Bruni D, Angell HK, Galon J (2020) The immune contexture and immunoscore in cancer prognosis and therapeutic efficacy. Nat Rev Cancer 20:662–680. https://doi.org/10.1038/s41568-020-0285-7

    Article  CAS  PubMed  Google Scholar 

  21. Chen Z, Liu X, Shang X, Qi K, Zhang S (2021) The diagnostic value of the combination of carcinoembryonic antigen, squamous cell carcinoma-related antigen, CYFRA 21–1, neuron-specific enolase, tissue polypeptide antigen, and progastrin-releasing peptide in small cell lung cancer discrimination. Int J Biol Markers 36:36–44. https://doi.org/10.1177/17246008211049446

    Article  CAS  PubMed  Google Scholar 

  22. Molina R, Filella X, Augé JM, Fuentes R et al (2003) Tumor markers (CEA, CA 125, CYFRA 21–1, SCC and NSE) in patients with non-small cell lung cancer as an aid in histological diagnosis and prognosis: comparison with the main clinical and pathological prognostic factors. Tumor Biol 24:209–218. https://doi.org/10.1159/000074432

    Article  CAS  Google Scholar 

  23. Boulanger M, Tual S, Lemarchand C, Guizard AV et al (2018) Diagnostic value of ProGRP for small cell lung cancer in different stages. J Thorac Dis 11:1182–1189. https://doi.org/10.21037/jtd.2019.04.29

    Article  Google Scholar 

  24. Oh HJ, Park HY, Kim KH, Park CK et al (2016) Progastrin-releasing peptide as a diagnostic and therapeutic biomarker of small cell lung cancer. J Thorac Dis 8:2530–2537. https://doi.org/10.21037/jtd.2016.08.72

    Article  PubMed  PubMed Central  Google Scholar 

  25. Maharjan A, Jo J, Acharya M, Yang S, Gautam R et al (2020) Quantitative association of humoral or cellular immunologic markers with the prediction of skewed adaptive immunity in agricultural workers. Quant Bio-Sci 39:111–117. https://doi.org/10.22283/qbs.2020.39.2.111

    Article  Google Scholar 

  26. Bray F, Ferlay J, Soerjomataram I, Siegel RL et al (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424. https://doi.org/10.3322/caac.21492

    Article  PubMed  Google Scholar 

  27. The National Lung Screening Trial Research Team (2011) Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 365:395–409. https://doi.org/10.1056/NEJMoa1102873

    Article  PubMed Central  Google Scholar 

  28. Seijo LM, Peled N, Ajona D, Boeri M et al (2019) Biomarkers in lung cancer screening: achievements, promises, and challenges. J Thorac Oncol 14:343–357. https://doi.org/10.1016/j.jtho.2018.11.023

    Article  CAS  PubMed  Google Scholar 

  29. Molina R, Marrades RM, Augé JM, Escudero JM et al (2016) Assessment of a combined panel of six serum tumor markers for lung cancer. Am J Respir Crit Care Med 193:427–437. https://doi.org/10.1164/rccm.201404-0603OC

    Article  CAS  PubMed  Google Scholar 

  30. Conway EM, Pikor LA, Kung SHY, Hamilton MJ et al (2016) Macrophages, inflammation, and lung cancer. Am J Respir Crit Care Med 193:116–130. https://doi.org/10.1164/rccm.201508-1545CI

    Article  CAS  PubMed  Google Scholar 

  31. Pernot S, Terme M, Radosevic-Robin N et al (2020) Infiltrating and peripheral immune cell analysis in advanced gastric cancer according to the Lauren classification and its prognostic significance. Gastric Cancer 23:73–81. https://doi.org/10.1007/s10120-019-00983-3

    Article  CAS  PubMed  Google Scholar 

  32. Krijgsman D, de Vries NL, Skovbo A, Andersen MN et al (2019) Characterization of circulating T-, NK-, and NKT cell subsets in patients with colorectal cancer: the peripheral blood immune cell profile. Cancer Immunol Immunother 68:1011–1024. https://doi.org/10.1007/s00262-019-02343-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wang WT, Zhu HY, Wu YJ, Xia Y et al (2018) Elevated absolute NK cell counts in peripheral blood predict good prognosis in chronic lymphocytic leukemia. J Cancer Res Clin Oncol 144:449–457. https://doi.org/10.1007/s00432-017-2568-2

    Article  PubMed  Google Scholar 

  34. Boulanger M, Tual S, Lemarchand C, Guizard AV et al (2018) Lung cancer risk and occupational exposures in crop farming: results from the AGRIculture and CANcer (AGRICAN) cohort. Occup Environ Med 75:776–785. https://doi.org/10.1136/oemed-2017-104976

    Article  PubMed  Google Scholar 

  35. Lee K, Lawson RJ, Olenchock SA, Vallyathan V et al (2004) Personal exposures to inorganic and organic dust in manual harvest of California citrus and table grapes. J Occup Environ Hyg 1:505–514. https://doi.org/10.1080/15459620490471616

    Article  CAS  PubMed  Google Scholar 

  36. Stapleton EM, O’Shaughnessy PT, Locke SJ et al (2018) A task-based analysis of black carbon exposure in Iowa farmers during harvest. J Occup Environ Hyg 15:293–304. https://doi.org/10.1080/15459624.2017.1422870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Coble J, Hoppin JA, Engel L, Elci OC et al (2002) Prevalence of exposure to solvents, metals, grain dust, and other hazards among farmers in the agricultural health study. J Expo Anal Environ Epidemiol 12:418–426. https://doi.org/10.1038/sj.jea.7500248

    Article  CAS  PubMed  Google Scholar 

  38. Lee WJ, Hoppin JA, Blair A, Lubin JH et al (2004) Cancer incidence among pesticide applicators exposed to alachlor in the agricultural health study. Am J Epidemiol 159:373–380. https://doi.org/10.1093/aje/kwoh040

    Article  PubMed  Google Scholar 

  39. Ha HY, Ra DS, Shin WC, Im GJ, Park JE (2012) Survey of pesticide use in fruit vegetables, fruits, and rice cultivation areas in Korea. Korean J Pestic Sci 16:395–400. https://doi.org/10.7585/kjps.2012.16.4.395

    Article  Google Scholar 

  40. Baldi I, Lebailly P, Bouvier G, Rondeau V et al (2014) Levels and determinants of pesticide exposure in re-entry workers in vineyards: results of the PESTEXPO study. Environ Res 132:360–369. https://doi.org/10.1016/j.envres.2014.04.035

    Article  CAS  PubMed  Google Scholar 

  41. Kasiotis KM, Tsakirakis AN, Richard Glass C, Charistou AN et al (2017) Assessment of field re-entry exposure to pesticides: a dislodgeable foliar residue study. Sci Total Environ 596:178–186. https://doi.org/10.1016/j.scitotenv.2017.04.016

    Article  CAS  PubMed  Google Scholar 

  42. Ben Khedher S, Neri M, Guida F, Matrat M et al (2017) Occupational exposure to endotoxins and lung cancer risk: results of the ICARE study. Occup Environ Med 74:667–679. https://doi.org/10.1136/oemed-2016-104117

    Article  PubMed  Google Scholar 

  43. Lenters V, Basinas I, Beane-Freeman L, Boffetta P et al (2010) Endotoxin exposure and lung cancer risk: a systematic review and meta-analysis of the published literature on agriculture and cotton textile workers. Cancer Causes Control 21:523–555. https://doi.org/10.1007/s10552-009-9483-z

    Article  PubMed  Google Scholar 

  44. Tewari A, Bedi J, Singh B, Gill JPS (2018) Oral exposure of deltamethrin and/or lipopolysaccharide (LPS) induced activation of the pulmonary immune system in Swiss albino mice. Environ Sci Pollut Res 25:15436–15448. https://doi.org/10.1007/s11356-018-1702-2

    Article  CAS  Google Scholar 

  45. Tewari A, Sethi RS, Banga HS et al (2017) Concomitant effect of low dose of lindane and intranasal lipopolysaccharide on respiratory system of mice. Hum Exp Toxicol 36:1201–1211. https://doi.org/10.1177/0960327116685889

    Article  CAS  PubMed  Google Scholar 

  46. Kim HA, Kim JY, Shin KM, Jo JH et al (2013) Relationship between endotoxin level of in swine farm dust and cellular immunity of husbandry workers. J Korean Soc Occup Environ Hyg 23:393–401

    Google Scholar 

  47. Baudoin W, Nono-Womdim R, Lutaladio N et al (2013) Good agricultural practices for greenhouse vegetable crops: principles for mediterranean climate areas. FAO Plant Production and Protection Paper 217, Food and Agriculture Organization of the United Nations, Rome

  48. Amoatey P, Al-Mayahi A, Omidvarborna H et al (2020) Occupational exposure to pesticides and associated health effects among greenhouse farm workers. Environ Sci Pollut Res Int 27:22251–22270. https://doi.org/10.1007/s11356-020-08754-9

    Article  CAS  PubMed  Google Scholar 

  49. Corrales L, Rosell R, Cardona AF et al (2020) Lung cancer in never smokers: the role of different risk factors other than tobacco smoking. Crit Rev Oncol Hematol 148:102895. https://doi.org/10.1016/j.critrevonc.2020.102895

    Article  PubMed  Google Scholar 

  50. Kim HC, Jung CY, Cho DG, Jeon JH et al (2019) Clinical characteristics and prognostic factors of lung cancer in Korea: a pilot study of data from the Korean nationwide lung cancer registry. Tuberc Respir Dis 82:118–125. https://doi.org/10.4046/trd.2017.0128

    Article  Google Scholar 

  51. Stapelfeld C, Dammann C, Maser E (2020) Sex-specificity in lung cancer risk. Int J Cancer 146:2376–2382. https://doi.org/10.1002/ijc.32716

    Article  CAS  PubMed  Google Scholar 

  52. Shi K, Li N, Yang M, Li W (2019) Identification of key genes and pathways in female lung cancer patients who never smoked by a bioinformatics analysis. J Cancer 10:51–60. https://doi.org/10.7150/jca.26908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Jung KW, Won YJ, Kang MJ et al (2022) Prediction of cancer incidence and mortality in Korea, 2022. Cancer Res Treat 54:345–351. https://doi.org/10.4143/crt.2022.179

    Article  PubMed  PubMed Central  Google Scholar 

  54. Lee J, Lim J, Kim Y, Kim HY et al (2019) Development of protocol for Korean lung cancer screening project (K-LUCAS) to evaluate effectiveness and feasibility to implement national cancer screening program. Cancer Res Treat 51:1285–1294. https://doi.org/10.4143/crt.2018.464

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the research grant from Daegu Catholic University (Grant no. 20201212).

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the research grant from Daegu Catholic University (Grant no. 20201212).

Author information

Authors and Affiliations

  1. Department of Occupational Health, College of Bio and Medical Sciences, Daegu Catholic University, 13-13, Hayang-Ro, Gyeongsan-Si, Gyeongsan, 38430, Republic of Korea

    Anju Maharjan, Ravi Gautam, Manju Acharya, JiHun Jo, DaEun Lee & Yong Heo

  2. Graduate School Department of Toxicology, Daegu Catholic University, Gyeongsan, 38430, Republic of Korea

    Pramod Bahadur K C, ChangYul Kim & Yong Heo

  3. Department of Food Science and Nutrition, College of Bio and Medical Sciences, Daegu Catholic University, 38430, Gyeongsan, Republic of Korea

    Young-A Lee

  4. Environmental Health Research Department, National Institute of Environmental Research, Incheon, 22689, Republic of Korea

    Jung-Taek Kwon

  5. Rural Development Administration, National Institute of Agricultural Sciences, Jeonju, 54875, Republic of Korea

    HyoCher Kim & KyungRan Kim

  6. Department of Preventive Medicine, College of Medicine, The Catholic University of Korea, Seoul, 06591, Republic of Korea

    HyoungAh Kim

Authors
  1. Anju Maharjan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ravi Gautam
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manju Acharya
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. JiHun Jo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. DaEun Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pramod Bahadur K C
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Young-A Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jung-Taek Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. HyoCher Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. KyungRan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. ChangYul Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. HyoungAh Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Yong Heo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Anju Maharjan, Ravi Gautam, Manju Acharya, JiHun Jo, DaeEun Lee, Pramod K C, Jung-Taek Kwon, HyoCher Kim, KyungRan Kim, ChangYul Kim, HyoungAh Kim, and Yong Heo. Funding acquisition was done by Young-A Lee and Yong Heo. The first draft of the manuscript was written by Anju Maharjan and Yong Heo and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yong Heo.

Ethics declarations

Conflict of interest

All authors declared no potential conflicts of interest to this article’s research, authorship, and/or publication.

Ethical approval

This study was performed following the approval of the Institutional Review Board of Daegu Catholic University (CUIRB-2019–0004/-01).

Consent to participate

Informed consent was obtained from all individual farmers included in the study.

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

Maharjan, A., Gautam, R., Acharya, M. et al. Association of immunotoxicological indices with lung cancer biomarkers in poultry, grape, and rose farming workers. Toxicol Res. 39, 739–747 (2023). https://doi.org/10.1007/s43188-023-00199-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s43188-023-00199-9

Keywords

Search

Navigation