Abstract
This report presents results from a study on the bacterial diversity of cigarette brands collected from military personnel during the U.S. Army’s investigation of a series of cases of acute eosinophilic pneumonitis in military personnel deployed in Operation Iraqi Freedom. Eight species of Bacillus, including five new species, and one new species of Kurthia were isolated from the cigarettes. Some of these species have been identified elsewhere as causes of hypersensitivity pneumonitis and other respiratory syndromes. All of the isolates were facultative anaerobes, and many displayed mucoid growth under anaerobic conditions. In addition, many isolates also displayed the ability to form surface biofilms under liquid culture. Although biofilm formation and mucoid growth were not correlated, the former was found to be much more pronounced under anaerobic conditions as opposed to aerobic ones. The implications of these findings are discussed.
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Literature Cited
JN Allen ER Pacht JE Gadek WB Davis (1989) ArticleTitleAcute eosinophilic pneumonia as a reversible cause of noninfectious respiratory failure N Engl J Med 321 569–574 Occurrence Handle2761601
C Ash JAE Farrow S Wallbanks MD Collins (1991) ArticleTitlePhylogenetic heterogeneity of the genus Bacillus revealed by comparative analysis of small-subunit-ribosomal RNA sequences Lett Appl Microbiol 13 202–206
WB Bekemeyer GA Zimmerman (1985) ArticleTitleLife threatening complications associated with Bacillus cereus pneumonia Am Rev Respir Dis 131 466–469 Occurrence Handle3919626
DI Bernstein ZL Lummus G Santilli J Siskosky IL Bernstein (1995) ArticleTitleMachine operator’s lung. A hypersensitivity pneumonitis disorder associated with exposure to metalworking fluid aerosols Chest 108 636–641 Occurrence Handle7656609
Blodgett R (2001) Most probable number determination from serial dilutions. Appendix 2. In: Bacteriological Analytical Manual. Center for Food Safety and Applied Nutrition, U.S. Food and Drug Administration, U.S. Department of Health and Human Services. [Online] http://www.cfsan.fda.gov/∼ebam/bam-toc.html
SS Branda JE González-Pastor S Ben-Yehuda R Losick R Kolter (2001) ArticleTitleFruiting body formation by Bacillus subtilis Proc Natl Acad Sci USA 98 11621–11626 Occurrence Handle10.1073/pnas.191384198 Occurrence Handle11572999
GE Carlisle 3rd JO Falkinham (1989) ArticleTitleEnzyme activities and antibiotic susceptibility of colonial variants of Bacillus subtilis and Bacillus licheniformis Appl Environ Microbiol 55 3026–3028 Occurrence Handle2483042
InstitutionalAuthorNameCenters for Disease Control (CDC) Prevention (2003) ArticleTitleSevere acute pneumonitis among deployed U.S. military personnel, Southwest Asia, March–August 2003 MMWR Morb Mortal Wkly Rep 52 857–859
J Chun KS Bae (2000) ArticleTitlePhylogenetic analysis of Bacillus subtilis and related taxa based on partial gyrA gene sequences Antonie Van Leeuwenhoek 78 123–127 Occurrence Handle10.1023/A:1026555830014 Occurrence Handle11204764
O Ciofu V Fussing N Bagge C Koch N Hoiby (2001) ArticleTitleCharacterization of paired mucoid/non-mucoid Pseudomonas aeruginosa isolates from Danish cystic fibrosis patients: antibiotic resistance, beta-lactamase activity and RiboPrinting J Antimicrob Chemother 48 391–396 Occurrence Handle10.1093/jac/48.3.391 Occurrence Handle11533004
T. Eaton JO Falkinham Suffix3rd CF Reyn Particlevon (1995) ArticleTitleRecovery of Mycobacterium avium from cigarettes J Clin Microbiol 33 2757–2758 Occurrence Handle8567919
ML Flindt DJ Hendrick (2002) ArticleTitlePapers that have changed the practice of occupational medicine: ‘Pulmonary disease due to inhalation of derivatives of Bacillus subtilis containing proteolytic enzyme’ by M.L.H. Flindt. 1969 Occup Med (Lond) 52 57–63
F Götz (2002) ArticleTitleStaphylococcus and biofilms Mol Microbiol 43 1367–1378 Occurrence Handle10.1046/j.1365-2958.2002.02827.x Occurrence Handle11952892
MA Hamon BA Lazazzera (2001) ArticleTitleThe sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis Mol Microbiol 42 1199–1209 Occurrence Handle10.1046/j.1365-2958.2001.02709.x Occurrence Handle11886552
DJ Hassett J Cuppoletti B Trapnell SV Lymar JJ Rowe SS Yoon GM Hilliard K Parvatiyar MC Kamani DJ Wozniak SH Hwang TR McDermott UA Ochsner (2002) ArticleTitleAnaerobic metabolism and quorum sensing by Pseudomonas aeruginosa biofilms in chronically infected cystic fibrosis airways: rethinking antibiotic treatment strategies and drug targets Adv Drug Deliv Rev 54 1425–1443 Occurrence Handle10.1016/S0169-409X(02)00152-7 Occurrence Handle12458153
CL Johnson IL Bernstein JS Gallagher PF Bonventre SM Brooks (1980) ArticleTitleFamilial hypersensitivity pneumonitis induced by Bacillus subtilis Am Rev Respir Dis 122 339–348 Occurrence Handle6774642
P Kaelin F Gadani (2000) ArticleTitleOccurrence of Bacillus thuringiensis on tobacco leaves Curr Microbiol 40 205–209 Occurrence Handle10.1007/s002849910041 Occurrence Handle10679055
M Kimura (1980) ArticleTitleA simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences J Mol Evol 16 111–120 Occurrence Handle7463489
JK Knobloch M Nedelmann K Kiel K Bartscht MA Horstkotte S Dobinsky H Rohde D Mack (2003) ArticleTitleEstablishment of an arbitrary PCR for rapid identification of Tn917 insertion sites in Staphylococcus epidermidis: characterization of biofilm-negative and non-mucoid mutants Appl Environ Microbiol 69 5812–5818 Occurrence Handle10.1128/AEM.69.10.5812-5818.2003 Occurrence Handle14532029
VP Kurup A Resnick SL Kagen SH Cohen JN Fink (1983) ArticleTitleAllergenic fungi and actinomycetes in smoking materials and their health implications Mycopathologia 82 61–64 Occurrence Handle10.1007/BF00436948 Occurrence Handle6348548
J-J Lu C-L Perng S-Y Li C-C Wan (2000) ArticleTitleUse of PCR with universal primers and restriction endonuclease digestions for detection and identification of common bacterial pathogens in cerebrospinal fluid J Clin Microbiol 38 2076–2080 Occurrence Handle10834956
JM Miller JG Hair M Hebert L Hebert Jr FJ Roberts RS Weyant (1997) ArticleTitleFulminating bacteremia and pneumonia due to Bacillus cereus J Clin Microbiol 35 504–507 Occurrence Handle9003628
M Nakajima T Manabe T Sasaki Y Niki T Matsushima (2000) ArticleTitleAcute eosinophilic pneumonia caused by cigarette smoking Intern Med 39 1131–1132 Occurrence Handle11197808
LK Nakamura MS Roberts FM Cohan (1999) ArticleTitleRelationship of Bacillus subtilis clades associated with strains 168 and W23: a proposal for Bacillus subtilis subsp. subtilis subsp. nov. and Bacillus subtilis subsp. spizizenii subsp. nov Int J Syst Bacteriol 49 1211–1215 Occurrence Handle10425781
SD Nightingale LT Byrd PM Southern JD Jockusch SX Cal BA Wynne (1992) ArticleTitleIncidence of Mycobacterium avium-intracellulare complex bacteremia in human immunodeficiency virus-positive patients J Infect Dis 165 1082–1085 Occurrence Handle1349906
M Reiman J Uitti (2000) ArticleTitleExposure to microbes, endotoxins and total dust in cigarette and cigar manufacturing: an evaluation of health hazards Ann Occup Hyg 44 467–473 Occurrence Handle10.1016/S0003-4878(00)00012-0 Occurrence Handle10963711
MS Roberts LK Nakamura FM Cohan (1994) ArticleTitleBacillus mojavensis sp. nov., distinguishable from Bacillus subtilis by sexual isolation, divergence in DNA sequence, and differences in fatty acid composition Int J Syst Bacteriol 44 256–264 Occurrence Handle8186089
MS Roberts LK Nakamura FM Cohan (1996) ArticleTitleBacillus vallismortis sp. nov., a close relative of Bacillus subtilis, isolated from soil in Death Valley, California Int J Syst Bacteriol 46 470–475 Occurrence Handle8934905
I Rubinstein GW Pedersen (2002) ArticleTitleBacillus species are present in chewing tobacco sold in the United States and evoke plasma exudation from the oral mucosa Clin Diagn Lab Immunol 9 1057–1060 Occurrence Handle10.1128/CDLI.9.5.1057-1060.2002 Occurrence Handle12204959
N Saitou M Nei (1987) ArticleTitleThe neighbor-joining method: a new method for reconstructing phylogenetic trees Mol Biol Evol 4 406–425 Occurrence Handle3447015
H Shintani M Fujimura M Yasui K Ueda S Kameda M Noto T Matsuda M Kobayashi (2000) ArticleTitleAcute eosinophilic pneumonia caused by cigarette smoking Intern Med 39 66–68 Occurrence Handle10674853
Y Shiota T Kawai H Matsumoto J Hiyama Y Tokuda M Marukawa T Ono H Mashiba (2000) ArticleTitleAcute eosinophilic pneumonia following cigarette smoking Intern Med 39 830–833 Occurrence Handle11030209
AF Shorr SL Scoville SB Cersovsky GD Shanks CF Ockenhouse BL Smoak WW Carr BP Petruccelli (2004) ArticleTitleAcute eosinophilic pneumonia among US Military personnel deployed in or near Iraq JAMA 292 2997–3005 Occurrence Handle10.1001/jama.292.24.2997 Occurrence Handle15613668
R Strauss A Mueller M Wehler D Neureiter E Fischer M Gramatzki EG Hahn (2001) ArticleTitlePseudomembranous tracheobronchitis due to Bacillus cereus Clin Infect Dis 33 E39–41 Occurrence Handle10.1086/322674 Occurrence Handle11486300
Y Tanino E Yamaguchi K Takaoka Y Fukui S Konno N Hizawa M Nishimura (2002) ArticleTitleCytokines and Th2 cells in AEP of smoking Allergy 57 463–464 Occurrence Handle10.1034/j.1398-9995.2002.23638.x
JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 25 4876–4882 Occurrence Handle10.1093/nar/25.24.4876 Occurrence Handle9396791
A Tripathi LC Grammer (2001) ArticleTitleExtrinsic allergic alveolitis from a proteolytic enzyme Ann Allergy Asthma Immunol 86 425–427 Occurrence Handle11345286
K Venkateswaran N Hattori MT La Duc R Kern (2003) ArticleTitleATP as a biomarker of viable microorganisms in clean-room facilities J Microbiol Methods 52 367–377 Occurrence Handle10.1016/S0167-7012(02)00192-6 Occurrence Handle12531506
K Watanabe M Fujimura K Kasahara M Yasui S Myou T Kita A Watanabe S Nakao (2002) ArticleTitleAcute eosinophilic pneumonia following cigarette smoking: a case report including cigarette-smoking challenge test Intern Med 41 1016–1020 Occurrence Handle12487181
E Wolinsky (1979) ArticleTitleNontuberculous mycobacteria and associated diseases Am Rev Respir Dis 119 107–159
Acknowledgments
We thank members of the USACHPPM investigation team for their contributions, especially J. Heller, R. Bowlus, and the field preventive medicine staff who collected the samples. We are grateful to H. Kline of the USDA-ARS for providing technical laboratory assistance and an anonymous reviewer for helpful comments. The mention of firm names or trade products does not imply that they are endorsed or recommended by the U.S. Department of Agriculture over other firms or similar products not mentioned. The opinions or assertions contained in this report are the views of the authors and are not to be construed as official or as reflecting the views of the U.S. Army, U.S. Department of Agriculture, or the U.S. Department of Defense.
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Rooney, A.P., Swezey, J.L., Wicklow, D.T. et al. Bacterial Species Diversity in Cigarettes Linked to an Investigation of Severe Pneumonitis in U.S. Military Personnel Deployed in Operation Iraqi Freedom. Curr Microbiol 51, 46–52 (2005). https://doi.org/10.1007/s00284-005-4491-z
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DOI: https://doi.org/10.1007/s00284-005-4491-z