RESEARCH PAPER
Acute hypersensitivity pneumonitis in woodworkers caused by inhalation of birch dust contaminated with Pantoea agglomerans and Microbacterium barkeri
| 1 | Department of Pneumonology, Oncology and Allergology, Medical University, Lublin, Poland |
| 2 | Department of Biological Health Hazards and Parasitology, Institute of Rural Health, Lublin, Poland |
| 3 | Department of Medical Radiology, Medical University, Lublin, Poland |
| 4 | Department of Immunology of Infectious Diseases, Hirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of Sciences, Wrocław, Poland |
| 5 | Department of Microbiology, Hirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of Sciences, Wrocław, Poland |
CORRESPONDING AUTHOR
Barbara Mackiewicz
Department of Pneumonology, Oncology and Allergology, Medical University, Lublin, Poland
Department of Pneumonology, Oncology and Allergology, Medical University, Lublin, Poland
Ann Agric Environ Med. 2019;26(4):644–655
KEYWORDS
hypersensitivity pneumonitiswood dustbacteriaPantoea agglomeransMicrobacterium barkeriinhalation challengeoccupational exposure
TOPICS
ABSTRACT
Case description:
Five workers (2 males and 3 females) employed in a furniture factory located in eastern Poland developed hypersensitivity pneumonitis (HP) after the pine wood used for furniture production was replaced by birch wood. All of them reported onset of respiratory and general symptoms (cough, shortness of breath, general malaise) after inhalation exposure to birch dust, showed crackles at auscultation, ground-glass attenuations in HRCT examination, and lymphocytosis in the BAL examination. The diagnosis of acute HP was set in 4 persons and the diagnosis of subacute HP in one.
Identification of specific allergen:
Samples of birch wood associated with evoking disease symptoms were subjected to microbiological analysis with the conventional and molecular methods. Two bacterial isolates were found to occur in large quantities (of the order 108 CFU/g) in examined samples: Gram-negative bacterium of the species Pantoea agglomerans and a non-filamentous Gram-positive actinobacterium of the species Microbacterium barkeri. In the test for inhibition of leukocyte migration, 4 out of 5 examined patients showed a positive reaction in the presence of P. agglomerans and 2 in the presence of M. barkeri. Only one person showed the presence of precipitins to P. agglomerans and none to M. barkeri. In the inhalation challenge, which is the most relevant allergological test in the HP diagnostics, all patients reacted positively to P. agglomerans and only one to M. barkeri. The results indicate that P. agglomerans developing in birch wood was the main agent causing HP in the workers exposed to the inhalation of dust from this wood, while the etiologic role of M. barkeri is probably secondary.
Conclusion:
The results demonstrate that apart from fungi and filamentous actinobacteria, regarded until recently as causative agents of HP in woodworkers, Gram-negative bacteria and non-filamentous actinobacteria may also elicit disease symptoms in the workers processing wood infected with large amounts of these microorganisms. The results obtained also seem to indicate that cellular-mediated reactions are more significant for causing disease symptoms compared to those that are precipitin-mediated.
Five workers (2 males and 3 females) employed in a furniture factory located in eastern Poland developed hypersensitivity pneumonitis (HP) after the pine wood used for furniture production was replaced by birch wood. All of them reported onset of respiratory and general symptoms (cough, shortness of breath, general malaise) after inhalation exposure to birch dust, showed crackles at auscultation, ground-glass attenuations in HRCT examination, and lymphocytosis in the BAL examination. The diagnosis of acute HP was set in 4 persons and the diagnosis of subacute HP in one.
Identification of specific allergen:
Samples of birch wood associated with evoking disease symptoms were subjected to microbiological analysis with the conventional and molecular methods. Two bacterial isolates were found to occur in large quantities (of the order 108 CFU/g) in examined samples: Gram-negative bacterium of the species Pantoea agglomerans and a non-filamentous Gram-positive actinobacterium of the species Microbacterium barkeri. In the test for inhibition of leukocyte migration, 4 out of 5 examined patients showed a positive reaction in the presence of P. agglomerans and 2 in the presence of M. barkeri. Only one person showed the presence of precipitins to P. agglomerans and none to M. barkeri. In the inhalation challenge, which is the most relevant allergological test in the HP diagnostics, all patients reacted positively to P. agglomerans and only one to M. barkeri. The results indicate that P. agglomerans developing in birch wood was the main agent causing HP in the workers exposed to the inhalation of dust from this wood, while the etiologic role of M. barkeri is probably secondary.
Conclusion:
The results demonstrate that apart from fungi and filamentous actinobacteria, regarded until recently as causative agents of HP in woodworkers, Gram-negative bacteria and non-filamentous actinobacteria may also elicit disease symptoms in the workers processing wood infected with large amounts of these microorganisms. The results obtained also seem to indicate that cellular-mediated reactions are more significant for causing disease symptoms compared to those that are precipitin-mediated.
REFERENCES (70)
1.
Selman M, Pardo A, King TE Jr. Hypersensitivity pneumonitis: insights in diagnosis and pathobiology. Am J Respir Crit Care Med. 2012; 186(4): 314–324.
2.
Spagnolo P, Rossi G, Cavazza A, Bonifazi M, Paladini I, Bonella F, Sverzellati N, Costabel U. Hypersensitivity pneumonitis: a comprehensive review. J Investig Allergol Clin Immunol. 2015; 25(4): 237–250.
3.
Quirce S, Vandenplas O, Campo P, Cruz MJ, de Blay F, Koschel D, Moscato G, Pala G, Raulf M, Sastre J, Siracusa A, Tarlo SM, Walusiak-Skorupa J, Cormier Y. Occupational hypersensitivity pneumonitis: an EAACI position paper. Allergy. 2016; 71(6): 765–779.
4.
Sforza GGR, Marinou A. Hypersensitivity pneumonitis: a complex lung disease. Clin Mol Allergy. 2017; 15:6.
5.
Greenberger PA. Hypersensitivity pneumonitis: a fibrosing alveolitis produced by inhalation of diverse antigens. J Allergy Clin Immunol. 2019; 143(4): 1295–1301.
6.
Nogueira R, Melo N, Novais e Bastos H, Martins N, Delgado L, Morais A, Mota PC. Hypersensitivity pneumonitis: Antigen diversity and disease implications. Pulmonology. 2019; 25(2): 97–108.
7.
National Institute for Occupational Safety and Health. Health effects of exposure to wood dust. A summary of the literature. U. S. Department of Health and Human Services, NIOSH Publication No. 00174745, Cincinnati, OH 1987.
8.
Kolmodin-Hedman B, Blomquist G, Lofgren F. Chipped wood as a source of mould exposure. Eur J Respir Dis. 1987; 71 (Suppl 154): S44–51.
9.
Johnson CL, Bernstein IL, Gallagher JS, Bonventre PF, Brooks SM. Familial hypersensitivity pneumonitis induced by Bacillus subtilis. Am Rev Respir Dis. 1980; 122: 339–348.
10.
Stone CA, Johnson GC, Thornton JD, Macauley BJ, Holmes PW, Tai EH. Leucogyrophana pinastri, a wood decay fungus as a probable cause of extrinsic allergic alveolitis syndrome. Aust NZ J Med. 1989; 19: 727–729.
11.
Bryant DH, Rogers P. Allergic alveolitis due to wood-rot fungi. Allergy Proc. 1991; 12(2): 89–94.
12.
Towey JW, Sweany HC, Huron WH. Severe bronchial asthma apparently due to fungus spores found in maple bark. JAMA. 1932; 99: 453–458.
13.
Emanuel DA, Wenzel FJ, Lawton BR. Pneumonitis due to Cryptostroma corticale (maple-bark disease). N Engl J Med. 1966; 274: 1413–1418.
14.
Ávila R, Lacey J. The role of Penicillium frequentans in suberosis. Clin Allergy. 1974; 4: 109–117.
15.
Belin L. Sawmill alveolitis in Sweden. Int Archs Allergy Appl Immun. 1987; 82: 440–443.
16.
Eduard W. Sandven P. Levy F. Exposure and IgG antibodies to mold spores in wood trimmers: exposure–response relationships with respiratory symptoms. Appl Occup Environ Hyg. 1994; 9: 44–48.
17.
Færden K, Lund MB, Mogens Aaløkken T, Eduard W, Søstrand P, Langård S, Kongerud J. Hypersensitivity pneumonitis in a cluster of sawmill workers: a 10-year follow-up of exposure, symptoms, and lung function. Int J Occup Environ Health. 2014; 20(2): 167–173.
18.
Van Assendelft AHW, Raitio M, Turkia V. Fuel chip-induced hypersensitivity pneumonitis caused by Penicillium species. Chest 1985; 87: 394–396.
19.
Dykewicz MS, Laufer P, Patterson R, Roberts M, Sommers HM. Woodman’s disease: Hypersensitivity pneumonitis from cutting live trees. J Allergy Clin Immunol. 1988; 81: 455–460.
20.
Winck JC, Delgado L, Murta R, Lopez M, Marques JA. Antigen characterization of major cork moulds in Suberosis (cork worker’s pneumonitis) by immunoblotting. Allergy. 2004; 59(7): 739–745.
21.
Minárik L, Mayer M, Votrubová V, Ürgeová N, Dutkiewicz J. Exogenous allergic alveolitis due to hypersensitivity to antigens from mouldy beechwood chips. Description of two cases. Studia Pneumol Phtiseol Cechoslov. 1983; 43: 38–45 (in Slovak).
22.
Halpin DMG, Graneek BJ, Turner-Warwick M, Newman-Taylor AJ. Extrinsic allergic alveolitis and asthma in a sawmill worker: case report and review of the literature. Occup Environ Med. 1994; 51: 160–164.
23.
Halpin DM, Graneek BJ, Lacey J, Nieuwenhuijsen MJ, Williamson PA, Venables KM, Newman Taylor AJ. Respiratory symptoms, immunological responses, and aeroallergen concentrations at a sawmill. Occup Environ Med. 1994; 51(3): 165–172.
24.
Cohen HI, Merigan TC, Kosek JC, Eldridge F. Sequoiosis. A granulomatous pneumonitis associated with redwood sawdust inhalation. Am J Med. 1967; 43: 785–794.
25.
Schlueter DP, Fink JN, Hensley GT. Wood-pulp worker’s disease: A hypersensitivity pneumonitis caused by Alternaria. Ann Intern Med. 1972; 77: 907–914.
26.
Veillette M, Cormier Y, Israël-Assayaq E, Meriaux A, Duchaine C. Hypersensitivity pneumonitis in a hardwood processing plant related to heavy mold exposure. J Occup Environ Hyg. 2006; 3: 301–307.
27.
Villar A, Muñoz X, Cruz MJ, Morell F. Hypersensitivity pneumonitis caused by Mucor species in a cork worker. Arch Bronconeumol. 2009; 45(8): 405–407 (in Spanish).
28.
Terho EO, Husman K, Kotimaa M, Sjöblom T. Extrinsic allergic alveolitis in a sawmill worker. A case report. Scand J Work Environ Health. 1980; 6: 153–157.
29.
Greene JG, Treuhaft MW, Arusell RM. Hypersensitivity pneumonitis due to Saccharomonospora viridis diagnosed by inhalation challenge. Ann Allergy. 1981; 47: 449–452.
30.
Baur X, Gahnz G, Chen Z. Extrinsic allergic alveolitis caused by cabreuva wood dust. J Allergy Clin Immunol. 2000; 106(4): 780–781.
31.
Meyer KC, Raghu G, Baughman RP, Brown KK, Costabel U, du Bois RM, Drent M, Haslam PL, KimDS, Nagai S, Rottoli P, Saltini C, Selman M, Strange C, Wood B. An official American Thoracic Society clinical practice guideline: the clinical utility of bronchoalveolar lavage cellular analysis in interstitial lung disease. Am J Respir Crit Care Med. 2012; 185(9): 1004–1014.
32.
Dutkiewicz J, Olenchock SA, Lewis DM, Ratajczak Z, Kwapiszewski C, Piech T, Bilczuk A. Drill samplers for quantification of microorganisms in wood. Forest Prod J. 1989; 39(2): 61–65.
33.
Milanowski J, Dutkiewicz J, Potoczna H, Kuś L, Urbanowicz B. Allergic alveolitis among agricultural workers in eastern Poland: A study of twenty cases. Ann Agric Environ Med; 1998; 5: 31–43.
34.
Holt JG, Krieg NR, Sneath PHA, Staley J, Williams ST. Bergey’s Manual of Determinative Bacteriology. 9 th Edition. Williams & Wilkins, Baltimore 1994.
35.
Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B. Food and Indoor Fungi. CBS-KNAV Fungal Biodiversity Centre, Utrecht, The Netherlands 2010.
36.
Watanabe T. Pictorial Atlas of Soil and Seed Fungi and Key to Species. 3 rd Edition, CRC Press, Taylor & Francis Group, Boca Raton, FL, 2010.
37.
Laron DH. Medically Important Fungi. A Guide to Identification. ASM Press, Washington, DC, 2011.
38.
Chun J, Goodfellow M. A phylogenetic analysis of the genus Nocardia with 16S rRNA gene sequences. Int J Syst Bacteriol. 1995; 45(2): 240–245.
39.
Paściak M, Dacko W, Sikora J, Gurlaga D, Pawlik K, Miękisiak G, Gamian A. Creation of an in-house Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry Corynebacterineae database overcomes difficulties in identification of Nocardia farcinica clinical isolates. J Clin Microbiol. 2015; 53: 2611–2621.
40.
Bowszyc J, Bowszyc J, Pawelec D. Test for leukocyte migration inhibition in whole blood capillary microcultures for evaluation of cellular immunity in tuberculosis. Gruźlica. 1975; 43: 369–374 (in Polish).
41.
Pepys J, Jenkins PA. Precipitin (F.L.H.) test in farmer’s lung. Thorax. 1965; 20: 21–35.
42.
Lacasse Y, Selman M, Costabel U, Dalphin JC, Morrel F, Erkinjuntti-Pekkanen R, Mueller NL, Colby TV, Schuyler M, Jomphe V, Cormier Y. HP Study Group: Classification of hypersensitivity pneumonitis: a hypothesis. Int Arch Allergy Immunol. 2009; 149: 161–166.
43.
Selman M. Hypersensitivity pneumonitis. In: Schwarz MI, King TJ Jr (Eds): Interstitial Lung Disease. BC Decker Publications, Hamilton (ON) 2003, 454–484.
44.
Lacasse Y, Selman M, Costabel U, Dalphin JC, Ando M, Morrel F, Erkinjuntti-Pekkanen R, Mueller NL, Colby TV, Schuyler M, Cormier Y. Clinical diagnosis of hypersensitivity pneumonitis. Am J Respir Crit Care Med. 2003; 168: 952–958.
45.
Girard M, Lacasse Y, Cormier Y. Hypersensitivity pneumonitis. Allergy. 2009; 64: 322–334.
46.
Girard M, Israël-Assayag E, Cormier Y. Pathogenesis of hypersensitivity pneumonitis. Curr Opin Allergy Clin Immunol. 2004; 4: 93–98.
47.
Määttä J, Lehto M, Leino M, Tillander S, Haapakoski R, Majuri M-L, Wolff H, Rautio S, Welling I, Husgafvel-Pursiainen K, Savolainen K, Alenius H. Mechanisms of particle-induced pulmonary inflammation in a mouse model: exposure to wood dust. Toxicol Sci 2006; 93(1): 96–104.
48.
Gustafson T, Dahlman-Höglund A, Nilsson K, Strömd K, Tornlinge G, Torén K. Occupational exposure and severe pulmonary fibrosis. Respir Med. 2007; 101: 2207–2212.
49.
Pepys J, Jenkins PA, Festenstein GN, Gregory PH, Lacey ME, Skinner FA. Farmer’s lung: thermophilic actinomycetes as a source of “farmer’s lung hay” antigen. Lancet. 1963; 2: 607–611.
50.
Rossell SE, Abbott EGM, Levy JF. Bacteria and wood. A review of the literature relating to the presence, action, and interaction of bacteria in wood. J Inst Wood Sci. 1973; 6(2): 28–35.
51.
Dutkiewicz J, Sorenson WG, Lewis DM, Olenchock SA. Levels of bacteria, fungi and endotoxin in stored timber. Int. Biodeterioration 1992; 30: 29–46.
52.
Dutkiewicz J.: Bacteria, fungi and endotoxin in stored timber logs and airborne sawdust in Poland. In: O’Rear CE, Llewellyn GC (Eds): Biodeterioration Research 2: General Biodeterioration, Degradation, Mycotoxins, Biotoxins, and Wood Decay, pp. 533–547. Plenum Press, New York 1989.
53.
Prażmo Z, Krysińska-Traczyk E, Skórska C, Sitkowska J, Cholewa G, Urbanowicz B, Dutkiewicz J. Birch wetwood as a source of potential bacterial hazard for woodworkers. Ann Agric Environ Med. 1996; 3: 67–70.
54.
Prażmo Z, Dutkiewicz J, Cholewa G. Gram-negative bacteria associated with timber as a potential respiratory hazard for woodworkers. Aerobiologia 2000; 16: 275–279.
55.
Prażmo Z, Dutkiewicz J. Gram-negative bacteria colonizing coniferous and deciduous wood. 1st Polish Scientific Conference „Biodeterioration of Technical Materials”, University of Technology, Łódź, 27 th January 2000, pp. 46–48 (in Polish).
56.
Wilson DA (Ed). Forensic Procedures for Boundary and Title Investigation. Appendix XII: Wood Identification. John Wiley & Sons, Inc., New York 2008.
57.
Dutkiewicz J, Mackiewicz B, Lemieszek MK, Golec M, Milanowski J. Pantoea agglomerans: a mysterious bacterium of evil and good. Part. I. Deleterious effects: Dust-borne endotoxins and allergens – focus on cotton dust. Ann Agric Environ Med. 2015; 22: 576–588.
58.
Dutkiewicz J, Mackiewicz B, Lemieszek M. Pantoea agglomerans: a mysterious bacterium of evil and good. LAP Lambert Academic Publishing, OmniScriptum GmbH & Co. KG, Saarbrücken, Germany 2017.
59.
Dutkiewicz J. Exposure to dust-borne bacteria in agriculture. I. Environmental studies. Arch Environ Health 1978; 33: 250–259.
60.
Dutkiewicz J., Mackiewicz B., Lemieszek M.K., Golec M., Skórska C., Góra-Florek A., Milanowski J.: Pantoea agglomerans: a mysterious bacterium of evil and good. Part. II. Deleterious effects: Dust-borne endotoxins and allergens – focus on grain dust, other agricultural dusts and wood dust. Ann Agric Environ Med. 2016; 23: 6–29.
61.
Kuś L. Allergic alveolitis after exposure to antigens occurring in grain dust in the light of own clinical and experimental investigations. Med Wiejska 1980; 15: 73–80 (in Polish).
62.
Kuś L. Allergic alveolitis after exposure to antigens occurring in grain dust in the light of own clinical and experimental investigations. Dissertation for the degree of Dr habil. Medical University, Lublin 1980 (in Polish).
63.
Mackiewicz B, Skórska C, Dutkiewicz J, Michnar M, Milanowski J, Prażmo Z, Krysińska-Traczyk E, Cisak E. Allergic alveolitis due to herb dust exposure. Ann Agric Environ Med. 1999; 6: 167–170.
64.
Sennekamp J, Joest M, Sander I, Engelhart S, Raulf-Heimsoth M. Farmer’s lung antigens in Germany. Pneumologie 2012; 66: 297–301.
65.
Dutkiewicz J.: Studies on endotoxins of Erwinia herbicola and their biological activity. Zbl Bakt Hyg I Abt Orig A 1976; 236: 487–508.
66.
Rylander R, Lundholm M. Bacterial contamination of cotton and cotton dust and effects on the lungs. Br J Ind Med. 1978; 35: 138–143.
67.
Rylander R, Bake B, Fischer JJ, Helander IM. Pulmonary function and symptoms after inhalation of endotoxin. Am Rev Respir Dis. 1989; 140: 981–986.
68.
Thorn J. The inflammatory response in humans after inhalation of bacterial endotoxin: a review. Inflamm Res. 2001; 50(5): 254–261.
69.
Pereira CAC, Gimenez A, Kuranishi L, Storrer K Chronic hypersensitivity pneumonitis. J Asthma Allergy 2016; 9: 171–181.
70.
Masuo M, Miyazaki Y, Suhara K, Ishizuka M, Fujie T, Inase N. Factors associated with positive inhalation provocation test results in subjects suspected of having chronic bird-related hypersensitivity pneumonitis. Respir Investig. 2016; 54(6): 454–461.
