Skip to main content

Advertisement

SpringerLink
Log in

Exposure to field vs. storage wheat dust: different consequences on respiratory symptoms and immune response among grain workers

  • Original Article
  • Published:
International Archives of Occupational and Environmental Health Aims and scope Submit manuscript

Abstract

Purpose

The aim of this study was to understand the differential acute effects of two distinct wheat-related dusts, such as field or stored wheat dust handling, on workers’ health and how those effects evolved at 6 month intervals.

Methods

Exposure, work-related symptoms, changes in lung function, and blood samples of 81 workers handling wheat and 61 controls were collected during the high exposure season and 6 months after. Specific IgG, IgE, and precipitins against 12 fungi isolated from wheat dust were titrated by enzyme-linked immunosorbent assay, dissociation-enhanced lanthanide fluorescence immunoassay, and electrosyneresis. The level of fungi was determined in the workers’ environment. Levels of exhaled fraction of nitrogen monoxide (FENO) and total IgE were obtained. Exposure response associations were investigated by mixed logistic and linear regression models.

Results

The recent exposure to field wheat dust was associated with a higher prevalence for five of six self-reported airway symptoms and with a lower FENO than those in the control population. Exposure to stored wheat dust was only associated with cough. No acute impact of exposure on respiratory function was observed. Exposure to field wheat dust led to workers’ sensitization against the three field fungi Aureobasidum, Cryptococcus, and Phoma, although exposure to storage wheat dust was associated with tolerance. The level of Ig remained stable 6 months after exposure.

Conclusion

The clinical picture of workers exposed to field or storage wheat dust differed. The systematic characterization of the aerosol microbial profile may help to understand the reasons for those differences.

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

Similar content being viewed by others

References

  • Barrera C, Richaud-Thiriez B, Rocchi S, Rognon B, Roussel S, Grenouillet F, Laboissiere A, Dalphin JC, Reboux G, Millon L (2016) New commercially available IgG kits and time-resolved fluorometric IgE assay for allergic broncho-pulmonary aspergillosis diagnosis in cystic fibrosis patients. Clin Vaccine Immunol 23:196–203

    Article  CAS  Google Scholar 

  • Basinas I, Schlünssen V, Heederik D, Sigsgaard T, Smit LAM, Samadi S, Omland Ø, Hjort C, Madsen AM, Skov S, Wouters IM (2012) Sensitisation to common allergens and respiratory symptoms in endotoxin exposed workers: a pooled analysis. Occup Environ Med 69:99–106

    Article  CAS  Google Scholar 

  • Camatini M, Corvaja V, Pezzolato E, Mantecca P, Gualtieri M (2012) PM10-biogenic fraction drives the seasonal variation of proinflammatory response in A549 cells. Environ Toxicol 27:63–73

    Article  CAS  Google Scholar 

  • Capasso L, Longhin E, Caloni F, Camatini M, Gualtieri M (2015) Synergistic inflammatory effect of PM10 with mycotoxin deoxynivalenol on human lung epithelial cells. Toxicon 104:65–72

    Article  CAS  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  Google Scholar 

  • Dalphin J-C, Reboux G, Lefebvre A, Thaon I (2009) Pneumopahties d’hypersensibilité. In: Traité de Pneumologie (ed) Flammarion, Paris

    Google Scholar 

  • Dannemiller KC, Gent JF, Leaderer BP, Peccia J (2016) Indoor microbial communities: influence on asthma severity in atopic and nonatopic children. J Allergy Clin Immunol 138:76–83

    Article  Google Scholar 

  • doPico GA, Reddan W, Anderson S, Flaherty D, Smalley E (1983) Acute effects of grain dust exposure during a work shift. Am Rev Respir Dis 128:399–404

    Article  CAS  Google Scholar 

  • Dorribo V, Wild P, Pralong JA, Danuser B, Reboux G, Krief P, Niculita-Hirzel H (2015) Respiratory health effects of fifteen years of improved collective protection in a wheat-processing worker population. Ann Agric Environ Med 22:647–654

    Article  Google Scholar 

  • Dweik RA, Boggs PB, Erzurum SC, Irvin CG, Leigh MW, Lundberg JO, Olin AC, Plummer AL, Taylor DR (2011) An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med 184:602–615

    Article  CAS  Google Scholar 

  • Eduard W, Pearce N, Douwes J (2009) Chronic bronchitis, COPD, and lung function in farmers: the role of biological agents. Chest 136:716–725

    Article  Google Scholar 

  • Flannigan B (1978) Primary contamination of barley and wheat grain storage fungi. Trans Br Mycol Soc 71:37–42

    Article  Google Scholar 

  • Gora A, Mackiewicz B, Krawczyk P, Golec M, Skorska C, Sitkowska J, Cholewa G, Larsson L, Jarosz M, Wojcik-Fatla A, Dutkiewicz J (2009) Occupational exposure to organic dust, microorganisms, endotoxin and peptidoglycan among plants processing workers in Poland. Ann Agric Environ Med 16:143 – 50

    Google Scholar 

  • Gualtieri M, Longhin E, Mattioli M, Mantecca P, Tinaglia V, Mangano E, Proverbio MC, Bestetti G, Camatini M, Battaglia C (2012) Gene expression profiling of A549 cells exposed to Milan PM2.5. Toxicol Lett 209:136–145

    Article  CAS  Google Scholar 

  • Halstensen AS, Heldal KK, Wouters IM, Skogstad M, Ellingsen DG, Eduard W (2013) Exposure to grain dust and microbial components in the Norwegian grain and compound feed industry. Ann Occup Hyg 57:1105–1114

    CAS  Google Scholar 

  • Instanes C, Hetland G (2004) Deoxynivalenol (DON) is toxic to human colonic, lung and monocytic cell lines, but does not increase the IgE response in a mouse model for allergy. Toxicology 204:13–21

    Article  CAS  Google Scholar 

  • Jagielo PJ, Thorne PS, Watt JL, Frees KL, Quinn TJ, Schwartz DA (1996) Grain dust and endotoxin inhalation challenges produce similar inflammatory responses in normal subjects. Chest 110:263–270

    Article  CAS  Google Scholar 

  • Jones M, Jeal H, Schofield S, Harris JM, Shamji MH, Francis JN, Durham SR, Cullinan P (2014) Rat-specific IgG and IgG4 antibodies associated with inhibition of IgE–allergen complex binding in laboratory animal workers. Occup Environ Med 71:619–623

    Article  CAS  Google Scholar 

  • Jouneau S, Boche A, Brinchault G, Fekete K, Guillot S, Bayat S, Desrues B (2012) On-site screening of farming-induced chronic obstructive pulmonary disease with the use of an electronic mini-spirometer: results of a pilot study in Brittany, France. Int Arch Occup Environ Health 85:623–630

    Article  Google Scholar 

  • Kankkunen P, Rintahaka J, Aalto A, Leino M, Majuri ML, Alenius H, Wolff H, Matikainen S (2009) Trichothecene mycotoxins activate inflammatory response in human macrophages. J Immunol 182:6418–6425

    Article  CAS  Google Scholar 

  • Katika MR, Hendriksen PJ, Shao J, van Loveren H, Peijnenburg A (2012) Transcriptome analysis of the human T lymphocyte cell line Jurkat and human peripheral blood mononuclear cells exposed to deoxynivalenol (DON): new mechanistic insights. Toxicol Appl Pharmacol 264:51–64

    Article  CAS  Google Scholar 

  • Kline JN, Jagielo PJ, Watt JL, Schwartz DA (2000) Bronchial hyperreactivity is associated with enhanced grain dust-induced airflow obstruction. J Appl Physiol 89:1172–1178

    Article  CAS  Google Scholar 

  • Kuhn DM, Ghannoum MA (2003) Indoor mold, toxigenic fungi, and Stachybotrys chartarum: infectious disease perspective. Clin Microbiol Rev 16:144–172

    Article  CAS  Google Scholar 

  • Le Bars J, Escoula L, Henry G (1973) Mycoflore des fourrages secs, Inventaire et fréquence des espèces. Ann Rech Vet 4:273–282

    Google Scholar 

  • Lucas D, Lodde B, Pougnet RP, Dewitte JD, Jegaden D (2013) Evaluation of the sensitisation to grains and its pulmonary impact in employees of the port of Brest silos. Int Marit Health 64:18–23

    Google Scholar 

  • Madsen AM, Zervas A, Tendal K, Nielsen JL (2015) Microbial diversity in bioaerosol samples causing ODTS compared to reference bioaerosol samples as measured using Illumina sequencing and MALDI-TOF. Environ Res 140:255–267

    Article  CAS  Google Scholar 

  • May S, Romberger DJ, Poole JA (2012) Respiratory health effects of large animal farming environments. J Toxicol Environ Health B Crit Rev 15:524–541

    Article  CAS  Google Scholar 

  • Minette A (1989) Questionnaire of the European Community for Coal and Steel (ECSC) on respiratory symptoms. 1987—updating of the 1962 and 1967 questionnaires for studying chronic bronchitis and emphysema. Eur Respir J 2:165–177

    CAS  Google Scholar 

  • Miyagawa T, Hamagami S, Tanigawa N (2000) Cryptococcus albidus-induced summer-type hypersensitivity pneumonitis. Am J Respir Crit Care Med 161:961–966

    Article  CAS  Google Scholar 

  • Moen BE, Kayumba A, Sakwari G, Mamuya SH, Bratveit M (2016) Endotoxin, dust and exhaled nitrogen oxide among hand pickers of coffee; a cross-sectional study. J Occup Med Toxicol 11:17

    Article  CAS  Google Scholar 

  • Moon Y, Pestka JJ (2002) Vomitoxin-induced cyclooxygenase-2 gene expression in macrophages mediated by activation of ERK and p38 but not JNK mitogen-activated protein kinases. Toxicol Sci 69:373–382

    Article  CAS  Google Scholar 

  • Moon Y, Pestka JJ (2003) Cyclooxygenase-2 mediates interleukin-6 upregulation by vomitoxin (deoxynivalenol) in vitro and in vivo. Toxicol Appl Pharmacol 187:80–88

    Article  CAS  Google Scholar 

  • Niculita-Hirzel H, Hantier G, Storti F, Plateel G, Roger T (2016) Frequent occupational exposure to Fusarium mycotoxins of workers in the Swiss grain industry. Toxins (Basel) 8:370

    Article  CAS  Google Scholar 

  • Noss I, Wouters IM, Visser M, Heederik DJ, Thorne PS, Brunekreef B, Doekes G (2008) Evaluation of a low-cost electrostatic dust fall collector for indoor air endotoxin exposure assessment. Appl Environ Microbiol 74:5621–5627

    Article  CAS  Google Scholar 

  • Pellissier L, Oppliger A, Hirzel AH, Savova-Bianchi D, Mbayo G, Mascher F, Kellenberger S, Niculita-Hirzel H (2016) Airborne and grain dust fungal community compositions are shaped regionally by plant genotypes and farming practices. Appl Environ Microbiol 82:2121–2131

    Article  CAS  Google Scholar 

  • Pitkaranta M, Meklin T, Hyvarinen A, Paulin L, Auvinen P, Nevalainen A, Rintala H (2008) Analysis of fungal flora in indoor dust by ribosomal DNA sequence analysis, quantitative PCR, and culture. Appl Environ Microbiol 74:233–244

    Article  CAS  Google Scholar 

  • Portengen L, Preller L, Tielen M, Doekes G, Heederik D (2005) Endotoxin exposure and atopic sensitization in adult pig farmers. J Allergy Clin Immunol 115:797–802

    Article  CAS  Google Scholar 

  • Rask-Andersen A (2011) Asthma increase among farmers: a 12-year follow-up. Ups J Med Sci 116,:60–71

    Article  Google Scholar 

  • Reboux G, Magy N, Dalphin JC, Gevois PA, De Vuyust P (2006) Immunological methods. In: Imaging of occupational and environmental disorders of the chest. Springer, Berlin, pp 133–158.

    Chapter  Google Scholar 

  • Reboux G, Piarroux R, Roussel S, Millon L, Bardonnet K, Dalphin JC (2007) Assessment of four serological techniques in the immunological diagnosis of farmers’ lung disease. J Med Microbiol 56:1317–1321

    Article  Google Scholar 

  • Roussel S, Rognon B, Barrera C, Reboux G, Salamin K, Grenouillet F, Thaon I, Dalphin J-C, Tillie-Leblond I, Quadroni M, Monod M, Millon L (2011a) Immuno-reactive proteins from Mycobacterium immunogenum useful for serodiagnosis of metalworking fluid hypersensitivity pneumonitis. Int J Med Microbiol 301:150–156

    Article  CAS  Google Scholar 

  • Roussel S, Sudre B, Reboux G, Waser M, Buchele G, Vacheyrou M, Dalphin JC, Millon L, Braun-Fahrlander C, von Mutius E, Piarroux R (2011b) Exposure to moulds and actinomycetes in Alpine farms: a nested environmental study of the PASTURE cohort. Environ Res 111:744–750

    Article  CAS  Google Scholar 

  • Schachter EN, Zuskin E, Rienzi N, Goswami S, Castranova V, Siegel P, Whitmer M, Chung E (2004) Pharmacological studies of the effect of wheat grain extract. Respiration 71:276–283

    Article  Google Scholar 

  • Scherer E, Rocchi S, Reboux G, Vandentorren S, Roussel S, Vacheyrou M, Raherison C, Millon L (2014) qPCR standard operating procedure for measuring microorganisms in dust from dwellings in large cohort studies. Sci Total Environ 466–467:716–724

    Article  CAS  Google Scholar 

  • Simon-Nobbe B, Denk U, Pöll V, Rid R, Breitenbach M (2008) The spectrum of fungal allergy. Int Arch Allergy Immunol 145:58–86

    Article  Google Scholar 

  • Smid T, Heederik D, Houba R, Quanjer PH (1994) Dust- and endotoxin-related acute lung function changes and work-related symptoms in workers in the animal feed industry. Am J Ind Med 25:877–888

    Article  CAS  Google Scholar 

  • Smit LA, Heederik D, Doekes G, Blom C, van Zweden I, Wouters IM (2008) Exposure–response analysis of allergy and respiratory symptoms in endotoxin-exposed adults. Eur Respir J 31:1241–1248

    Article  CAS  Google Scholar 

  • Spankie S, Cherrie JW (2012) Exposure to grain dust in Great Britain. Ann Occup Hyg 56:25–36

    CAS  Google Scholar 

  • Straumfors A, Heldal KK, Wouters IM, Eduard W (2015) Work tasks as determinants of grain dust and microbial exposure in the Norwegian grain and compound feed industry. Ann Occup Hyg 59:724–736

    Article  CAS  Google Scholar 

  • Straumfors A, Heldal KK, Eduard W, Wouters IM, Ellingsen DG, Skogstad M (2016) Cross-shift study of exposure–response relationships between bioaerosol exposure and respiratory effects in the Norwegian grain and animal feed production industry. Occup Environ Med 73:685–693

    Article  Google Scholar 

  • Sundblad BM, Larsson BM, Palmberg L, Larsson K (2002) Exhaled nitric oxide and bronchial responsiveness in healthy subjects exposed to organic dust. Eur Respir J 20:426–431

    Article  CAS  Google Scholar 

  • Sundblad BM, von Scheele I, Palmberg L, Olsson M, Larsson K (2009) Repeated exposure to organic material alters inflammatory and physiological airway responses. Eur Respir J 34:80–88

    Article  CAS  Google Scholar 

  • Swan JR, Crook B (1998) Airborne microorganisms associated with grain handling. Ann Agric Environ Med 5:7–15

    CAS  Google Scholar 

  • Vacher G, Niculita-Hirzel H, Roger T (2015) Immune responses to airborne fungi and non-invasive airway diseases. Semin Immunopathol 37:83–96

    Article  CAS  Google Scholar 

  • Viet SM, Buchan R, Stallones L (2001) Acute respiratory effects and endotoxin exposure during wheat harvest in Northeastern Colorado. Appl Occup Environ Hyg 16:685–697

    Article  CAS  Google Scholar 

  • Wiszniewska M, Tymoszuk D, Nowakowska-ŚWirta E, PaŁCzyŃSki C, Walusiak-Skorupa J (2013) Mould Sensitisation among bakers and farmers with work-related respiratory symptoms. Ind Health 51:275–284

    Article  Google Scholar 

  • Xu X, Hu H, Kearney GD, Kan H, Carrillo G, Chen X (2016) A population-based study of smoking, serum cotinine and exhaled nitric oxide among asthmatics and a healthy population in the USA. Inhal Toxicol 28:724–730

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank Dr. C. Lazor-Blanchet and M. Coté for their support recruiting the controls, M. Porchet and D. Spinedi for helping with data collection, Y. Randin for data management supportand BioMed Proofreading® LLC experts to correct the English.

Funding

The study was funded by the ANSES (Agence Nationale de Sécurité Sanitaire de l’Alimentation, de l’Environnement et du Travail, France) Grant 2011/1/087 to HNH and by a SUVA (Caisse nationale suisse d’assurance en cas d’accidents) grant to PK and BD. The funding organs played no role in the collection of data, formulation of study hypothesis analyses, or interpretation of findings.

Author information

Authors and Affiliations

  1. UMR6249 Chrono-Environnement, University of Franche-Comté, Besançon, France

    Coralie Barrera, Audrey Laboissière, Laurence Millon & Gabriel Reboux

  2. Parasitology-Mycology Department, University Hospital of Besançon, Besançon, France

    Coralie Barrera, Audrey Laboissière, Laurence Millon & Gabriel Reboux

  3. Service of Occupational Hygiene, Institute for Work and Health, University of Lausanne and Geneva, Epalinges-Lausanne, Switzerland

    Pascal Wild, Dessislava Savova-Bianchi & Hélène Niculita-Hirzel

  4. Scientific Management, INRS, Nancy, France

    Pascal Wild

  5. Service of Occupational Medicine, Institute for Work and Health, University of Lausanne and Geneva, Epalinges-Lausanne, Switzerland

    Victor Dorribo, Jacques A. Pralong, Brigitta Danuser & Peggy Krief

Authors
  1. Coralie Barrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pascal Wild
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Victor Dorribo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dessislava Savova-Bianchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Audrey Laboissière
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jacques A. Pralong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Brigitta Danuser
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Peggy Krief
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Laurence Millon
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Gabriel Reboux
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hélène Niculita-Hirzel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hélène Niculita-Hirzel.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 25 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barrera, C., Wild, P., Dorribo, V. et al. Exposure to field vs. storage wheat dust: different consequences on respiratory symptoms and immune response among grain workers. Int Arch Occup Environ Health 91, 745–757 (2018). https://doi.org/10.1007/s00420-018-1322-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00420-018-1322-7

Keywords

Search

Navigation