Asia Pac Allergy.  2014 Apr;4(2):91-98. 10.5415/apallergy.2014.4.2.91.

Association of airborne Aspergillus with asthma exacerbation in Southern Pakistan

• Zubairi AB
• Azam I
• Awan S
• Zafar A
• Imam AA

• KMID: 2397111
• DOI: http://doi.org/10.5415/apallergy.2014.4.2.91

Abstract

BACKGROUND
Exposure to airborne fungi has been related with exacerbation of asthma in adults and children leading to increased outpatient, emergency room visits, and hospitalizations. Hypersensitivity to these airborne fungi may be an important initial predisposing factor in the development and exacerbation of asthma.
OBJECTIVE
This study was conducted to determine an association between fungal types and spore concentrations with the risk of asthma exacerbation in adults.
METHODS
This cross-sectional study was conducted from May 2008 to August 2009 at the Aga Khan University Hospital Karachi, Pakistan. All adult (age≥16 years) patients presenting to the hospital with acute asthma exacerbation were enrolled after informed consent. A home survey was conducted for each patient to assess their environmental characteristics. Indoor air samples were also obtained from the patient's home to determine the type and spore concentration of fungi within the week of their enrollment in the study.
RESULTS
Three hundred and ninety-one patients with an acute asthma exacerbation were enrolled during the study period. The mean age of participants was 46 years (standard deviation, ±18 years) and 247 (63.2%) were females. A trend of higher asthma enrollment associated with higher Aspergillus concentrations was found in two consecutive summers. A total of nineteen types of fungi were found in air samples. Aspergillus spp. was the most frequently isolated fungus with acute asthma exacerbation.
CONCLUSION
An association of higher concentration of indoor Aspergillus spp. with asthma exacerbation in adults was observed in this study.

Keyword

Aspergillus; Asthma; Fungal spores; Pakistan

MeSH Terms

Adult
Aspergillus*
Asthma*
Causality
Child
Cross-Sectional Studies
Emergency Service, Hospital
Female
Fungi
Hospitalization
Humans
Hypersensitivity
Informed Consent
Outpatients
Pakistan*
Spores
Spores, Fungal

Figure

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  Fig. 1 Map of Karachi city showing areas of outdoor and indoor sampling. Outdoor samples. Areas of patient enrollment.

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  Fig. 2 Flow chart of the study.

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  Fig. 3 Relationship between enrollment of asthma exacerbation, humidity and indoor Aspergillus concentration.

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  Fig. 4 Relationship between enrollment due to asthma exacerbation and indoor spores concentration.

Reference

1. Knutsen AP, Bush RK, Demain JG, Denning DW, Dixit A, Fairs A, Greenberger PA, Kariuki B, Kita H, Kurup VP, Moss RB, Niven RM, Pashley CH, Slavin RG, Vijay HM, Wardlaw AJ. Fungi and allergic lower respiratory tract diseases. J Allergy Clin Immunol. 2012; 129:280–291.

2. Rosenstreich DL, Eggleston P, Kattan M, Baker D, Slavin RG, Gergen P, Mitchell H, McNiff-Mortimer K, Lynn H, Ownby D, Malveaux F. The role of cockroach allergy and exposure to cockroach allergen in causing morbidity among inner-city children with asthma. N Engl J Med. 1997; 336:1356–1363.

3. O'Hollaren MT, Yunginger JW, Offord KP, Somers MJ, O'Connell EJ, Ballard DJ, Sachs MI. Exposure to an aeroallergen as a possible precipitating factor in respiratory arrest in young patients with asthma. N Engl J Med. 1991; 324:359–363.

4. Targonski PV, Persky VW, Ramekrishnan V. Effect of environmental molds on risk of death from asthma during the pollen season. J Allergy Clin Immunol. 1995; 95(5 Pt 1):955–961.

5. Black PN, Udy AA, Brodie SM. Sensitivity to fungal allergens is a risk factor for life-threatening asthma. Allergy. 2000; 55:501–504.

6. Cruz AA, Bousquet J, Khaltaev NG. Global surveillance, prevention and control of chronic respiratory diseases: a comprehensive approach. Geneva: World Health Organization;2007.

7. Kalliel JN, Goldstein BM, Braman SS, Settipane GA. High frequency of atopic asthma in a pulmonary clinic population. Chest. 1989; 96:1336–1340.

8. Institute of Medicine (US). Committee on Damp Indoor Spaces and Health. Damp indoor spaces and health. Washington, DC: National Academies Press;2004.

9. Douwes J, Pearce N. Invited commentary: is indoor mold exposure a risk factor for asthma? Am J Epidemiol. 2003; 158:203–206.

10. Salo PM, Arbes SJ Jr, Sever M, Jaramillo R, Cohn RD, London SJ, Zeldin DC. Exposure to Alternaria alternata in US homes is associated with asthma symptoms. J Allergy Clin Immunol. 2006; 118:892–898.

11. Bush RK, Prochnau JJ. Alternaria-induced asthma. J Allergy Clin Immunol. 2004; 113:227–234.

12. Pulimood TB, Corden JM, Bryden C, Sharples L, Nasser SM. Epidemic asthma and the role of the fungal mold Alternaria alternata. J Allergy Clin Immunol. 2007; 120:610–617.

13. O'connor GT, Walter M, Mitchell H, Kattan M, Morgan WJ, Gruchalla RS, Pongracic JA, Smartt E, Stout JW, Evans R, Crain EF, Burge HA. Airborne fungi in the homes of children with asthma in low-income urban communities: The Inner-City Asthma Study. J Allergy Clin Immunol. 2004; 114:599–606.

14. Bernton HS. Asthma due to a mold-aspergillus fumigatus. JAMA. 1930; 95:189–191.

15. Rhodes HL, Thomas P, Sporik R, Holgate ST, Cogswell JJ. A birth cohort study of subjects at risk of atopy: twenty-two-year followup of wheeze and atopic status. Am J Respir Crit Care Med. 2002; 165:176–180.

16. Singh AM, Busse WW. Asthma exacerbations. 2: aetiology. Thorax. 2006; 61:809–816.

17. Zureik M, Neukirch C, Leynaert B, Liard R, Bousquet J, Neukirch F. European Community Respiratory Health Survey. Sensitisation to airborne moulds and severity of asthma: cross sectional study from European Community respiratory health survey. BMJ. 2002; 325:411–414.

18. Hinson KF, Moon AJ, Plummer NS. Broncho-pulmonary aspergillosis; a review and a report of eight new cases. Thorax. 1952; 7:317–333.

19. Schwartz HJ, Greenberger PA. The prevalence of allergic bronchopulmonary aspergillosis in patients with asthma, determined by serologic and radiologic criteria in patients at risk. J Lab Clin Med. 1991; 117:138–142.

20. Maurya V, Gugnani HC, Sarma PU, Madan T, Shah A. Sensitization to Aspergillus antigens and occurrence of allergic bronchopulmonary aspergillosis in patients with asthma. Chest. 2005; 127:1252–1259.

21. Denning DW, O'Driscoll BR, Hogaboam CM, Bowyer P, Niven RM. The link between fungi and severe asthma: a summary of the evidence. Eur Respir J. 2006; 27:615–626.

22. Kauffman HF, Tomee JF, van de Riet MA, Timmerman AJ, Borger P. Protease-dependent activation of epithelial cells by fungal allergens leads to morphologic changes and cytokine production. J Allergy Clin Immunol. 2000; 105(6 Pt 1):1185–1193.

23. Agarwal R, Gupta D. Severe asthma and fungi: current evidence. Med Mycol. 2011; 49:Suppl 1. S150–S157.

24. Rao TA, Shaikh AH, Ahmed M. Airborne fungal flora of Karachi, Pakistan. Pak J Bot. 2009; 41:1421–1428.

25. Afzal M, Mehdi FS. Atmospheric fungi of Karachi city. Pak J Biol Sci. 2002; 5:707–709.

26. The Global Initiative for Asthma. GINA report: global strategy for asthma management and prevention. Updated 2012 [Internet]. The global initiative for asthma;c2012. cited 2012 Dec 10. Available from: http://www.ginasthma.org/documents/4.

27. Pakistan Meteorological Department, Government of Pakistan [Internet]. Islamabad: Pakistan Meteorological Department, Government of Pakistan;c2012. 2012 Dec 10. Available from: http://www.pmd.gov.pk/.

28. Shendell DG, Mizan SS, Yamamoto N, Peccia J. Associations between quantitative measures of fungi in home floor dust and lung function among older adults with chronic respiratory disease: a pilot study. J Asthma. 2012; 49:502–509.

29. Dales RE, Cakmak S, Burnett RT, Judek S, Coates F, Brook JR. Influence of ambient fungal spores on emergency visits for asthma to a regional children's hospital. Am J Respir Crit Care Med. 2000; 162:2087–2090.

30. Atkinson RW, Strachan DP, Anderson HR, Hajat S, Emberlin J. Temporal associations between daily counts of fungal spores and asthma exacerbations. Occup Environ Med. 2006; 63:580–590.

31. Rosas I, McCartney HA, Payne RW, Calderon C, Lacey J, Chapela R, Ruiz-Velazco S. Analysis of the relationships between environmental factors (aeroallergens, air pollution, and weather) and asthma emergency admissions to a hospital in Mexico City. Allergy. 1998; 53:394–401.

32. Nicholson KG, Kent J, Ireland DC. Respiratory viruses and exacerbations of asthma in adults. BMJ. 1993; 307:982–986.

33. Johnston NW. The similarities and differences of epidemic cycles of chronic obstructive pulmonary disease and asthma exacerbations. Proc Am Thorac Soc. 2007; 4:591–596.

34. Fisk WJ, Lei-Gomez Q, Mendell MJ. Meta-analyses of the associations of respiratory health effects with dampness and mold in homes. Indoor Air. 2007; 17:284–296.

35. Mendell MJ, Mirer AG, Cheung K, Tong M, Douwes J. Respiratory and allergic health effects of dampness, mold, and dampness-related agents: a review of the epidemiologic evidence. Environ Health Perspect. 2011; 119:748–756.

36. Siddiqui AR, Lee K, Gold EB, Bhutta ZA. Eye and respiratory symptoms among women exposed to wood smoke emitted from indoor cooking: a study from southern pakistan. Energy Sustain Dev. 2005; 9:58–66.

37. Chen Y, Stewart P, Johansen H, McRae L, Taylor G. Sex difference in hospitalization due to asthma in relation to age. J Clin Epidemiol. 2003; 56:180–187.

38. Schatz M, Clark S, Camargo CA Jr. Sex differences in the presentation and course of asthma hospitalizations. Chest. 2006; 129:50–55.