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

  • Coralie Barrera
  • Pascal Wild
  • Victor Dorribo
  • Dessislava Savova-Bianchi
  • Audrey Laboissière
  • Jacques A. Pralong
  • Brigitta Danuser
  • Peggy Krief
  • Laurence Millon
  • Gabriel Reboux
  • Hélène Niculita-Hirzel
Original Article



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.


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.


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.


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.


Grain workers Cattle raisers Respiratory symptoms Occupational wheat dust exposure Fungi-specific immunoglobulins 



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.


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.

Compliance with ethical standards

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.

Supplementary material

420_2018_1322_MOESM1_ESM.docx (24 kb)
Supplementary material 1 (DOCX 25 KB)


  1. 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 23:196–203CrossRefGoogle Scholar
  2. 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 69:99–106CrossRefGoogle Scholar
  3. 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 27:63–73CrossRefGoogle Scholar
  4. 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 104:65–72CrossRefGoogle Scholar
  5. 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 7:335–336CrossRefGoogle Scholar
  6. Dalphin J-C, Reboux G, Lefebvre A, Thaon I (2009) Pneumopahties d’hypersensibilité. In: Traité de Pneumologie (ed) Flammarion, ParisGoogle Scholar
  7. 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 138:76–83CrossRefGoogle Scholar
  8. 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 128:399–404CrossRefGoogle Scholar
  9. 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 22:647–654CrossRefGoogle Scholar
  10. 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 184:602–615CrossRefGoogle Scholar
  11. Eduard W, Pearce N, Douwes J (2009) Chronic bronchitis, COPD, and lung function in farmers: the role of biological agents. Chest 136:716–725CrossRefGoogle Scholar
  12. Flannigan B (1978) Primary contamination of barley and wheat grain storage fungi. Trans Br Mycol Soc 71:37–42CrossRefGoogle Scholar
  13. 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 – 50Google Scholar
  14. 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 209:136–145CrossRefGoogle Scholar
  15. 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 57:1105–1114Google Scholar
  16. 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 204:13–21CrossRefGoogle Scholar
  17. 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 110:263–270CrossRefGoogle Scholar
  18. 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 71:619–623CrossRefGoogle Scholar
  19. 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 85:623–630CrossRefGoogle Scholar
  20. 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 182:6418–6425CrossRefGoogle Scholar
  21. 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 264:51–64CrossRefGoogle Scholar
  22. Kline JN, Jagielo PJ, Watt JL, Schwartz DA (2000) Bronchial hyperreactivity is associated with enhanced grain dust-induced airflow obstruction. J Appl Physiol 89:1172–1178CrossRefGoogle Scholar
  23. Kuhn DM, Ghannoum MA (2003) Indoor mold, toxigenic fungi, and Stachybotrys chartarum: infectious disease perspective. Clin Microbiol Rev 16:144–172CrossRefGoogle Scholar
  24. Le Bars J, Escoula L, Henry G (1973) Mycoflore des fourrages secs, Inventaire et fréquence des espèces. Ann Rech Vet 4:273–282Google Scholar
  25. 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 64:18–23Google Scholar
  26. 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 140:255–267CrossRefGoogle Scholar
  27. May S, Romberger DJ, Poole JA (2012) Respiratory health effects of large animal farming environments. J Toxicol Environ Health B Crit Rev 15:524–541CrossRefGoogle Scholar
  28. 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 2:165–177Google Scholar
  29. Miyagawa T, Hamagami S, Tanigawa N (2000) Cryptococcus albidus-induced summer-type hypersensitivity pneumonitis. Am J Respir Crit Care Med 161:961–966CrossRefGoogle Scholar
  30. 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 11:17CrossRefGoogle Scholar
  31. 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 69:373–382CrossRefGoogle Scholar
  32. Moon Y, Pestka JJ (2003) Cyclooxygenase-2 mediates interleukin-6 upregulation by vomitoxin (deoxynivalenol) in vitro and in vivo. Toxicol Appl Pharmacol 187:80–88CrossRefGoogle Scholar
  33. 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) 8:370CrossRefGoogle Scholar
  34. 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 74:5621–5627CrossRefGoogle Scholar
  35. 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 82:2121–2131CrossRefGoogle Scholar
  36. 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 74:233–244CrossRefGoogle Scholar
  37. Portengen L, Preller L, Tielen M, Doekes G, Heederik D (2005) Endotoxin exposure and atopic sensitization in adult pig farmers. J Allergy Clin Immunol 115:797–802CrossRefGoogle Scholar
  38. Rask-Andersen A (2011) Asthma increase among farmers: a 12-year follow-up. Ups J Med Sci 116,:60–71CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. 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 56:1317–1321CrossRefGoogle Scholar
  41. 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 301:150–156CrossRefGoogle Scholar
  42. 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 111:744–750CrossRefGoogle Scholar
  43. 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 71:276–283CrossRefGoogle Scholar
  44. 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 466–467:716–724CrossRefGoogle Scholar
  45. Simon-Nobbe B, Denk U, Pöll V, Rid R, Breitenbach M (2008) The spectrum of fungal allergy. Int Arch Allergy Immunol 145:58–86CrossRefGoogle Scholar
  46. 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 25:877–888CrossRefGoogle Scholar
  47. 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 31:1241–1248CrossRefGoogle Scholar
  48. Spankie S, Cherrie JW (2012) Exposure to grain dust in Great Britain. Ann Occup Hyg 56:25–36Google Scholar
  49. 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 59:724–736CrossRefGoogle Scholar
  50. 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 73:685–693CrossRefGoogle Scholar
  51. 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 20:426–431CrossRefGoogle Scholar
  52. 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 34:80–88CrossRefGoogle Scholar
  53. Swan JR, Crook B (1998) Airborne microorganisms associated with grain handling. Ann Agric Environ Med 5:7–15Google Scholar
  54. Vacher G, Niculita-Hirzel H, Roger T (2015) Immune responses to airborne fungi and non-invasive airway diseases. Semin Immunopathol 37:83–96CrossRefGoogle Scholar
  55. Viet SM, Buchan R, Stallones L (2001) Acute respiratory effects and endotoxin exposure during wheat harvest in Northeastern Colorado. Appl Occup Environ Hyg 16:685–697CrossRefGoogle Scholar
  56. 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 51:275–284CrossRefGoogle Scholar
  57. 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 28:724–730CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Coralie Barrera
    • 1
    • 2
  • Pascal Wild
    • 3
    • 4
  • Victor Dorribo
    • 5
  • Dessislava Savova-Bianchi
    • 3
  • Audrey Laboissière
    • 1
    • 2
  • Jacques A. Pralong
    • 5
  • Brigitta Danuser
    • 5
  • Peggy Krief
    • 5
  • Laurence Millon
    • 1
    • 2
  • Gabriel Reboux
    • 1
    • 2
  • Hélène Niculita-Hirzel
    • 3
  1. 1.UMR6249 Chrono-EnvironnementUniversity of Franche-ComtéBesançonFrance
  2. 2.Parasitology-Mycology DepartmentUniversity Hospital of BesançonBesançonFrance
  3. 3.Service of Occupational Hygiene, Institute for Work and HealthUniversity of Lausanne and GenevaEpalinges-LausanneSwitzerland
  4. 4.Scientific ManagementINRSNancyFrance
  5. 5.Service of Occupational Medicine, Institute for Work and HealthUniversity of Lausanne and GenevaEpalinges-LausanneSwitzerland

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