Indoor fungal diversity and asthma: A meta-analysis and systematic review of risk factors

Journal of Allergy and Clinical Immunology

Volumn 135, Issue 1, 2015, Pages 110-122

  Sharpe, Richard A ^a   Bearman, Nick ^a,b   Thornton, Christopher R ^c   Husk, Kerryn ^a   Osborne, Nicholas J ^a,d  

^a UNIVERSITY OF EXETER MEDICAL SCHOOL   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c UNIVERSITY OF EXETER   (United Kingdom)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

damp; indoor fungi and allergic asthma; Systematic review

Indexed keywords

AIR SAMPLING; ALLERGIC ASTHMA; ALTERNARIA; AMBIENT AIR; ARTICLE; ASPERGILLUS; ASTHMA; CLADOSPORIUM; DISEASE EXACERBATION; FUNGAL CONTAMINATION; FUNGUS GROWTH; HEALTH HAZARD; HUMAN; MICROBIAL DIVERSITY; MOISTURE; NONHUMAN; PENICILLIUM; SPECIES DIVERSITY; SUSCEPTIBLE POPULATION; SYSTEMATIC REVIEW; AIR POLLUTANT; CLASSIFICATION; ENVIRONMENTAL EXPOSURE; FUNGUS; INDOOR AIR POLLUTION; ISOLATION AND PURIFICATION; META ANALYSIS; RISK FACTOR;

AIR POLLUTANT;

AIR POLLUTANTS; AIR POLLUTION, INDOOR; ASTHMA; ENVIRONMENTAL EXPOSURE; FUNGI; HUMANS; RISK FACTORS;

EID: 84920400541     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2014.07.002     Document Type: Article

References (76)

1. M.I. Asher, S. Montefort, B. Björkstén, C.K. Lai, D.P. Strachan, and S.K. Weiland Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys Lancet 368 2006 733 743
2. T. To, S. Stanojevic, G. Moores, A.S. Gershon, E.D. Bateman, and A.A. Cruz Global asthma prevalence in adults: findings from the cross-sectional world health survey BMC Public Health 12 2012 204
3. E. von Mutius The environmental predictors of allergic disease J Allergy Clin Immunol 105 2000 9 19
4. C.S. Barnes, N.E. Alexis, J.A. Bernstein, J.R. Cohn, J.G. Demain, and E. Horner Climate change and our environment: the effect on respiratory and allergic disease J Allergy Clin Immunol Pract 1 2013 137 141
5. Environmental Protection Agency. Public health consequences and cost of climate change impacts on indoor environments. Washington: Available at: http://www.epa.gov/iaq/pdfs/mudarri.pdf. Accessed January 26, 2014.
6. P. Wilkinson, K.R. Smith, S. Beevers, C. Tonne, and T. Oreszczyn Energy, energy efficiency, and the built environment Lancet 370 2007 1175 1187
7. J. Lavergea, N. Van Den Bosschea, N. Heijmansb, and A. Janssensa Energy saving potential and repercussions on indoor air quality of demand controlled residential ventilation strategies Building Environ 46 2011 1497 1503
8. R. Sharpe, C.R. Thornton, and N.J. Osborne Modifiable factors governing indoor fungal diversity and risk of asthma Clin Exp Allergy 44 2014 631 641
9. G. Weinmayr, U. Gehring, J. Genuneit, G. Büchele, A. Kleiner, and R. Siebers Dampness and moulds in relation to respiratory and allergic symptoms in children: results from Phase Two of the International Study of Asthma and Allergies in Childhood (ISAAC Phase Two) Clin Exp Allergy 43 2013 762 774
10. R. Quansah, M.S. Jaakkola, T.T. Hugg, S.A.M. Heikkinen, and J.J.K. Jaakkola Residential dampness and molds and the risk of developing asthma: a systematic review and meta-analysis PLoS One 7 2012 e47526
11. W.J. Fisk, Q. Lei-Gomez, and M.J. Mendell Meta-analyses of the associations of respiratory health effects with dampness and mold in homes Indoor Air 17 2007 284 296
12. M.J. Mendell, A.G. Mirer, K. Cheung, M. Tong, and J. Douwes Respiratory and allergic health effects of dampness, mold, and dampness-related agents: a review of the epidemiologic evidence Environ Health Perspect 119 2011 748 756
13. T. Reponen, L. Levin, S. Zheng, S. Vesper, P. Ryan, and S.A. Grinshpun Family and home characteristics correlate with mold in homes Environ Res 124 2013 67 70
14. A. Fairs, A.J. Wardlaw, Thompson Jr., and C.H. Pashley Guidelines on ambient intramural airborne fungal spores J Investig Allergol Clin Immunol 20 2010 490 498
15. S. Gravesen, P.A. Nielsen, R. Iversen, and K.F. Nielsen Microfungal contamination of damp buildings - examples of risk constructions and risk materials Environ Health Perspect 107 1999 505 508
16. T. Reponen, J. Lockey, D.I. Bernstein, S.J. Vesper, L. Levin, and G.K.K. Hershey Infant origins of childhood asthma associated with specific molds J Allergy Clin Immunol 130 2012 639 644
17. R.I. Adams, M. Miletto, J.W. Taylor, and T.D. Bruns Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances ISME J 7 2013 1262 1273
18. B. Simon-Nobbe, U. Denk, V. Pöll, R. Rid, and M. Breitenbach The spectrum of fungal allergy Int Arch Allergy Immunol 145 2008 58 86
19. S. Vesper, J. Wakefield, P. Ashley, D. Cox, G. Dewalt, and W. Friedman Geographic distribution of Environmental Relative Moldiness Index molds in USA homes J Environ Public Health 2011 2011 242457
20. S. Ja Cho, G. Ramachandran, S. Banerjee, A.D. Ryan, and J.L. Adgate Seasonal variability of culturable fungal genera in the house dust of inner-city residences J Occup Environ Hyg 5 2008 780 789
21. M. Frankel, G. Bekö, M. Timm, S. Gustavsen, E.W. Hansen, and A.M. Madsen Seasonal variations of indoor microbial exposures and their relation to temperature, relative humidity, and air exchange rate Appl Environ Microbiol 78 2012 8289 8297
22. M.I. Asher, U. Keil, H.R. Anderson, R. Beasley, J. Crane, and F. Martinez International Study of Asthma and Allergies in Childhood (ISAAC): rationale and methods Eur Respir J 8 1995 483 491
23. K.F. Chung, S.E. Wenzel, J.L. Brozek, A. Bush, M. Castro, and P.J. Sterk International ERS/ATS guidelines on definition, evaluation and treatment of severe asthma Eur Respir J 43 2014 343 373
24. J. Agbetile, A. Fairs, D. Desai, B. Hargadon, M. Bourne, and K. Mutalithas Isolation of filamentous fungi from sputum in asthma is associated with reduced post-bronchodilator FEV1 Clin Exp Allergy 42 2012 782 791
25. R. Crameri, M. Garbani, C. Rhyner, and C. Huitema Fungi: the neglected allergenic sources Allergy 69 2014 176 185
26. Y. Matsuwaki, K. Wada, T. White, H. Moriyama, and H. Kita Alternaria fungus induces the production of GM-CSF, interleukin-6 and interleukin-8 and calcium signaling in human airway epithelium through protease-activated receptor 2 Int Arch Allergy Immunol 158 suppl 1 2012 19 29
27. Thomson-Reuters. Endnote. US, 2012.
28. D. Moher, A. Liberati, J. Tetzlaff, and D.G. Altman Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement J Clin Epidemiol 62 2009 1006 1012
29. The Newcastle-Ottawa Scale (NOS) for assessing the quality if nonrandomized studies in meta-analyses. Available at: http://www.ohri.ca/programs/clinical-epidemiology/oxford.asp. Accessed April 11, 2013.
30. P.M. Salo, S.J. Arbes Jr., M. Sever, R. Jaramillo, R.D. Cohn, and S.J. London Exposure to Alternaria alternata in US homes is associated with asthma symptoms J Allergy Clin Immunol 118 2006 892 898
31. A. Araki, A. Kanazawa, T. Kawai, Y. Eitaki, K. Morimoto, and K. Nakayama The relationship between exposure to microbial volatile organic compound and allergy prevalence in single-family homes Sci Total Environ 423 2012 18 26
32. R.E. Dales, D. Miller, and J. White Testing the association between residential fungus and health using ergosterol measures and cough recordings Mycopathologia 147 1999 21 27
33. R. Jones, G.M. Recer, S.A. Hwang, and S. Lin Association between indoor mold and asthma among children in Buffalo, New York Indoor Air 21 2011 156 164
34. C.S. Li, and L.Y. Hsu Airborne fungus allergen in association with residential characteristics in atopic and control children in a subtropical region Arch Environ Health 52 1997 72 79
35. P.F. Rosenbaum, J.A. Crawford, S.E. Anagnost, C.J.K. Wang, A. Hunt, and R.D. Anbar Indoor airborne fungi and wheeze in the first year of life among a cohort of infants at risk for asthma J Expo Sci Environ Epidemiol 20 2010 503 515
36. S. Dharmage, M. Bailey, J. Raven, T. Mitakakis, A. Cheng, and D. Guest Current indoor allergen levels of fungi and cats, but not house dust mites, influence allergy and asthma in adults with high dust mite exposure Am J Respir Crit Care Med 164 2001 65 71
37. Cochrane Handbook. Chapter 9: analysing data and undertaking meta-analyses. Available at: http://hiv.cochrane.org/sites/hiv.cochrane.org/files/uploads/Ch09-Analysing.pdf. Accessed October 18, 2013.
38. R. DerSimonian, and N. Laird Meta-analysis in clinical trials Control Clin Trials 7 1986 177 188
39. M. Matheson, M.J. Abramson, S.C. Dharmage, A.B. Forbes, J.M. Raven, and F.C.K. Thien Changes in indoor allergen and fungal levels predict changes in asthma activity among young adults Clin Exp Allergy 35 2005 907 913
40. S.J. Vesper, C. McKinstry, Y. Chin, R.A. Haugland, C.M. Kercsmar, and I. Yike Specific molds associated with asthma in water-damaged homes J Occup Environ Med 48 2006 852 858
41. D.P. Strachan, B. Flannigan, E.M. McCabe, and F. McGarry Quantification of airborne moulds in the homes of children with and without wheeze Thorax 45 1990 382 387
42. J. Holme, L. Hagerhed-Engman, J. Mattsson, J. Sundell, and C.G. Bornehag Culturable mold in indoor air and its association with moisture-related problems and asthma and allergy among Swedish children Indoor Air 20 2010 329 340
43. S. Vesper, C. McKinstry, R. Haugland, L. Neas, E. Hudgens, and B. Heidenfelder Higher Environmental Relative Moldiness Index (ERMIsm) values measured in Detroit homes of severely asthmatic children Sci Total Environ 394 2008 192 196
44. H.-J. Su, P.-C. Wu, H.-L. Chen, F.-C. Lee, and L.-L. Lin Exposure assessment of indoor allergens, endotoxin, and airborne fungi for homes in southern Taiwan Environ Res 85 2001 135 144
45. J. Meng, C.S. Barnes, and L.J. Rosenwasser Identity of the fungal species present in the homes of asthmatic children Clin Exp Allergy 42 2012 1448 1458
46. J.F. Gent, R. Ping, K. Belanger, E. Triche, M.B. Bracken, and T.R. Holford Levels of household mold associated with respiratory symptoms in the first year of life in a cohort at risk for asthma Environ Health Perspect 110 2002 A781
47. A.B. Herrera, L.A. Rodríguez, and J. Niederbacher [Biological pollution and its relationship with respiratory symptoms indicative of asthma, Bucaramanga, Colombia.] Biomedica 31 2011 357 371
48. S.J. Vesper, C. McKinstry, C. Yang, R.A. Haugland, C.M. Kercsmar, and I. Yike Specific molds associated with asthma in water-damaged homes J Occup Environ Med 48 2006 852 858
49. S. Vesper, C. McKinstry, R. Haugland, L. Wymer, K. Bradham, and P. Ashley Development of an Environmental Relative Moldiness Index for US Homes J Occup Environ Med 49 2007 829 833
50. S. Vesper Traditional mould analysis compared to a DNA-based method of mould analysis Crit Rev Microbiol 37 2011 15 24
51. D. Méheust, P. Le Cann, G. Reboux, L. Millon, and J.-P. Gangneux Indoor fungal contamination: health risks and measurement methods in hospitals, homes and workplaces Crit Rev Microbiol 40 2014 248 260
52. G.L. Chew, C. Rogers, H.A. Burge, M.L. Muilenberg, and D.R. Gold Dustborne and airborne fungal propagules represent a different spectrum of fungi with differing relations to home characteristics Allergy 58 2003 13 20
53. A.V. Arundel, E.M. Sterling, J.H. Biggin, and T.D. Sterling Indirect health effects of relative humidity in indoor environments Environ Health Perspect 65 1986 351
54. J. Gaffin, and W. Phipatanakul The role of indoor allergens in the development of asthma Curr Opin Allergy Clin Immunol 9 2009 128 135
55. J.D. Bufford, C.L. Reardon, Z. Li, K.A. Roberg, D. DaSilva, and P.A. Eggleston Effects of dog ownership in early childhood on immune development and atopic diseases Clin Exp Allergy 38 2008 1635 1643
56. S. Fernández-Rodríguez, R. Tormo-Molina, J.M. Maya-Manzano, I. Silva-Palacios, and Á. Gonzalo-Garijo Outdoor airborne fungi captured by viable and non-viable methods Fungal Ecol 7 2014 16 26
57. C.H. Pashley, A. Fairs, R.C. Free, and A.J. Wardlaw DNA analysis of outdoor air reveals a high degree of fungal diversity, temporal variability, and genera not seen by spore morphology Fungal Biol 116 2012 214 224
58. J.J. Jaakkola, B.F. Hwang, and N. Jaakkola Home dampness and molds, parental atopy, and asthma in childhood: a six-year population-based cohort study Environ Health Perspect 113 2005 357 361
59. M.S. Jaakkola, H. Nordman, R. Piipari, J. Uitti, J. Laitinen, and A. Karjalainen Indoor dampness and molds and development of adult-onset asthma: a population-based incident case-control study Environ Health Perspect 110 2002 543 547
60. R. Sharma, R. Deval, V. Priyadarshi, S.N. Gaur, V.P. Singh, and A.B. Singh Indoor fungal concentration in the homes of allergic/asthmatic children in Delhi, India [published erratum appears in Allergy Rhinol (Providence) 2011;2):e62] Allergy Rhinol 2 2011 21 32
61. P.D. Blanc, P.J. Quinlan, P.P. Katz, J.R. Balmes, L. Trupin, and M.G. Cisternas Higher environmental relative moldiness index values measured in homes of adults with asthma, rhinitis, or both conditions Environ Res 122 2013 98 101
62. J.D. Hayes, M.A. Jhaveri, D.M. Mannino, H. Strawbridge, and J. Temprano The effect of mold sensitization and humidity upon allergic asthma Clin Respir J 7 2012 135 144
63. M. Zureik, C. Neukirch, B. Leynaert, R. Liard, J. Bousquet, and F. Neukirch Sensitisation to airborne moulds and severity of asthma: cross sectional study from European Community respiratory health survey BMJ 325 2002 411
64. T.B. Pulimood, J.M. Corden, C. Bryden, L. Sharples, and S.M. Nasser Epidemic asthma and the role of the fungal mold Alternaria alternata J Allergy Clin Immunol 120 2007 610 617
65. M.S. Jaakkola, A. Ieromnimon, and J.J.K. Jaakkola Are atopy and specific IgE to mites and molds important for adult asthma? J Allergy Clin Immunol 117 2006 642 648
66. J.A. Pongracic, G.T. O'Connor, M.L. Muilenberg, B. Vaughn, D.R. Gold, and M. Kattan Differential effects of outdoor versus indoor fungal spores on asthma morbidity in inner-city children J Allergy Clin Immunol 125 2010 593 599
67. K.W. Bundy, J.F. Gent, W. Beckett, M.B. Bracken, K. Belanger, and E. Triche Household airborne Penicillium associated with peak expiratory flow variability in asthmatic children Ann Allergy Asthma Immunol 103 2009 26 30
68. M. Turyk, L. Curtis, P. Scheff, A. Contraras, L. Coover, and E. Hernandez Environmental allergens and asthma morbidity in low-income children J Asthma 43 2006 453 457
69. J.F. Gent, J.M. Kezik, M.E. Hill, E. Tsai, D.-W. Li, and B.P. Leaderer Household mold and dust allergens: Exposure, sensitization and childhood asthma morbidity Environ Res 118 2012 86 93
70. R. Agarwal, and D. Gupta Severe asthma and fungi: current evidence Med Mycol 49 suppl 2011 S150 S157
71. S. Nasser, and T. Pulimood Allergens and thunderstorm asthma Curr Allergy Asthma Rep 9 2009 384 390
72. D. Denning, C. Pashley, D. Hartl, A. Wardlaw, C. Godet, and S. Del Giacco Fungal allergy in asthma-state of the art and research needs Clin Transl Allergy 4 2014 14
73. P.M. Salo, S.J. Arbes Jr., P.W. Crockett, P.S. Thorne, R.D. Cohn, and D.C. Zeldin Exposure to multiple indoor allergens in US homes and its relationship to asthma J Allergy Clin Immunol 121 2008 678 684.e2
74. D. Heederik, and E. von Mutius Does diversity of environmental microbial exposure matter for the occurrence of allergy and asthma? J Allergy Clin Immunol 130 2012 44 50
75. C. Crawford, T. Reponen, T. Lee, Y. Iossifova, L. Levin, and A. Adhikari Temporal and spatial variation of indoor and outdoor airborne fungal spores, pollen, and (1→3)-β-D-glucan Aerobiologia 25 2009 147 158
76. M. Larsson, L. Hägerhed-Engman, S. Moniruzzaman, S. Janson, J. Sundell, and C.-G. Bornehag Can we trust cross-sectional studies when studying the risk of moisture-related problems indoor for asthma in children? Int J Environ Health Res 21 2011 237 247