Synergism between allergens and viruses and risk of hospital admission with asthma: case-control study
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Abstract Objective: To investigate the importance of sensitisation and exposure to allergens and viral infection in precipitating acute asthma in adults resulting in admission to hospital. Design: Case-control study. Setting: Large district general hospital. Participants: 60 patients aged 17-50 admitted to hospital over a year with acute asthma, matched with two controls: patients with stable asthma recruited from the outpatient department and patients admitted to hospital with non-respiratory conditions (inpatient controls). Main outcome measures: Atopic status (skin testing and total and specific IgE), presence of common respiratory viruses and atypical bacteria (polymerase chain reaction), dust samples from homes, and exposure to allergens (enzyme linked immunosorbent assay (ELISA): Der p 1, Fel d 1, Can f 1, and Bla g 2). Results: Viruses were detected in 31 of 177 patients. The difference in the frequency of viruses detected between the groups was significant (admitted with asthma 26%, stable asthma 18%, inpatient controls 9%; P=0.04). A significantly higher proportion of patients admitted with asthma (66%) were sensitised and exposed to either mite, cat, or dog allergen than patients with stable asthma (37%) and inpatient controls (15%; P<0.001). Being sensitised and exposed to allergens was an independent associate of the group admitted to hospital (odds ratio 2.3, 95% confidence interval 1.0 to 5.4; P=0.05), whereas the combination of sensitisation, high exposure to one or more allergens, and viral detection considerably increased the risk of being admitted with asthma (8.4, 2.1 to 32.8; P=0.002). Conclusions: Allergens and viruses may act together to exacerbate asthma. What is already known on this topic Studies on segmental allergen challenge of the lung and experimental rhinovirus infection show synergistic effects between allergens and respiratory virus infection No studies have investigated an interaction between sensitisation, exposure to allergens, and virus infections in real life exacerbations of asthma What this study adds Allergens and viruses may act together to exacerbate asthma, indicating that domestic exposure to allergens acts synergistically with viruses in sensitised patients, increasing the risk of hospital admission Strategies to reduce the impact of asthma exacerbations in adults should include interventions directed at both viruses and reducing exposure to allergens
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The synergism between allergic sensitization, high allergen exposure, and viral infection (mostly rhinovirus) increases the risk of hospitalization in adults with asthma.
“The synergism between allergic sensitization, high allergen exposure, and viral infection (mostly rhinovirus) has been shown to increase the risk of hospitalization, both in children (52) and in adults (81) with asthma.”
From Epidemiology of Asthma in Children and Adults (2019) · cites this paper as [81]
Cites
Community study of role of viral infections in exacerbations of asthma in 9–11 year old children
Johnston, S. L., Pattemore, P. K., Sanderson, G., Smith, S., Lampe, F., Josephs, L., Symington, P., Toole, S. O., Myint, S. H., Tyrrell, D. A. J., et al. (1995) · BMJ · doi:10.1136/bmj.310.6989.1225 · Cited by 1,991 · see citing works
Self-citationRosenstreich, D. L., Eggleston, P., Kattan, M., Baker, D., Slavin, R. G., Gergen, P., Mitchell, H., McNiff-Mortimer, K., Lynn, H., Ownby, D., et al. (1997) · New England Journal of Medicine · doi:10.1056/nejm199705083361904 · Cited by 1,380 · see citing works
Respiratory viruses and exacerbations of asthma in adults
Nicholson, K. G., Kent, J., & Ireland, D. C. (1993) · BMJ · doi:10.1136/bmj.307.6910.982 · Cited by 1,127 · see citing works
Indoor allergens and asthma:Report of the Third International Workshop
Platts‐Mills, T. A. E., VERVLOET, D., Thomas, W. R., Aalberse, R. C., & Chapman, M. D. (1997) · Journal of Allergy and Clinical Immunology · doi:10.1016/s0091-6749(97)70292-6 · Cited by 723 · see citing works
Johnston, S. L., Pattemore, P., Sanderson, G., Smith, S. H., Campbell, M. J., Josephs, L. K., Cunningham, A. F., Robinson, B. S., Myint, S., Ward, M. E., et al. (1996) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.154.3.8810601 · Cited by 563 · see citing works
Self-citationA National Estimate of the Economic Costs of Asthma
SMITH, D. H., MALONE, D. C., Lawson, K. A., Okamoto, L. J., Battista, C., & Saunders, W. B. (1997) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.156.3.9611072 · Cited by 562 · see citing works
Gelber, L. E., Seltzer, L. H., Bouzoukis, J. K., Pollart, S. M., Chapman, M. D., & Platts‐Mills, T. A. E. (1993) · American Review of Respiratory Disease · doi:10.1164/ajrccm/147.3.573 · Cited by 463 · see citing works
Lemanske, R. F., Dick, E. C., Swenson, C. A., Vrtis, R. F., & Busse, W. W. (1989) · Journal of Clinical Investigation · doi:10.1172/jci113843 · Cited by 413 · see citing works
Luczynska, C. M., Arruda, L. K., Platts‐Mills, T. A. E., Miller, J. D., Lopez, M., & Chapman, M. D. (1989) · Journal of Immunological Methods · doi:10.1016/0022-1759(89)90010-0 · Cited by 403 · see citing works
Lower Airways Inflammation during Rhinovirus Colds in Normal and in Asthmatic Subjects
Fraenkel, D. J., Bardin, P. G., Sanderson, G., Lampe, F. C., Johnston, S. L., & Holgate, S. T. (1995) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm/151.3_pt_1.879 · Cited by 387 · see citing works
Self-citationIngram, J. M., Sporik, R. B., Rose, G., Honsinger, R. W., Chapman, M. D., & Platts‐Mills, T. A. E. (1995) · Journal of Allergy and Clinical Immunology · doi:10.1016/s0091-6749(95)70286-5 · Cited by 308 · see citing works
Calhoun, W. J., Dick, E. C., Schwartz, L. B., & Busse, W. W. (1994) · Journal of Clinical Investigation · doi:10.1172/jci117581 · Cited by 300 · see citing works
Chapman, M. D., Aalberse, R. C., Brown, M. J., & Platts‐Mills, T. A. E. (1988) · The Journal of Immunology · doi:10.4049/jimmunol.140.3.812 · Cited by 297 · see citing works
Duff, A. L., Pomeranz, E. S., Gelber, L. E., Price, G. W., Farris, H., Hayden, F. G., Platts‐Mills, T. A. E., & Heymann, P. W. (1993) · PEDIATRICS · doi:10.1542/peds.92.4.535 · Cited by 286 · see citing works
T1 and T2 CD4+ cells in human allergic diseases
Umetsu, D. T., & DeKruyff, R. H. (1997) · Journal of Allergy and Clinical Immunology · doi:10.1016/s0091-6749(97)70186-6 · Cited by 273 · see citing works
Exposure to house dust mite allergens and the clinical activity of asthma
Custovic, A., Taggart, S. C. O., Francis, H. C., Chapman, M. D., & Woodcock, A. (1996) · Journal of Allergy and Clinical Immunology · doi:10.1016/s0091-6749(96)70227-0 · Cited by 251 · see citing works
Self-citationExperimental Rhinovirus 16 Infection
Grünberg, K., Smits, H. H., Timmers, M. C., de Klerk, E. P. A., Dolhain, R. J. E. M., Dick, E. C., Hiemstra, P. S., & Sterk, P. J. (1997) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.156.2.9610079 · Cited by 188 · see citing works
Custovic, A., Green, R., Fletcher, A., Smith, A., Pickering, C., Chapman, M., & Woodcock, A. (1997) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.155.1.9001295 · Cited by 179 · see citing works
Self-citationMonoclonal antibodies to the major feline allergen Fel d I
de Groot, H., van Swieten, P., van Leeuwen, J., Lind, P., & Aalberse, R. C. (1988) · Journal of Allergy and Clinical Immunology · doi:10.1016/0091-6749(88)90079-6 · Cited by 128 · see citing works
Identification, quantitation, and purification of cockroach allergens using monoclonal antibodies
Pollart, S. M., Mullins, D., Vailes, L. D., Hayden, M. L., Platts‐Mills, T. A. E., Sutherland, W. M., & Chapman, M. D. (1991) · Journal of Allergy and Clinical Immunology · doi:10.1016/0091-6749(91)90010-l · Cited by 124 · see citing works
Sensitivity and exposure to indoor allergens in adults with differing asthma severity
Tunnicliffe, W. S., Fletcher, T., Hammond, K., Roberts, K., Čustović, A., Simpson, A., Woodcock, A. A., & Ayres, J. G. (1999) · European Respiratory Journal · doi:10.1183/09031936.99.13365499 · Cited by 119 · see citing works
Self-citationSimpson, A., Čustović, A., Pipis, S., Adisesh, A., Faragher, B. E., & Woodcock, A. A. (1999) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.160.1.9809091 · Cited by 94 · see citing works
Self-citationBusse, W. W., & Gern, J. E. (1997) · Journal of Allergy and Clinical Immunology · doi:10.1016/s0091-6749(97)70216-1 · Cited by 56 · see citing works
Campbell, M. J., Holgate, S. T., & Johnston, S. L. (1997) · BMJ · doi:10.1136/bmj.315.7114.1012 · Cited by 54 · see citing works
Self-citation
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Epidemiology of Asthma in Children and Adults
Dharmage, S. C., Perret, J. L., & Custovic, A. (2019) · Frontiers in Pediatrics · doi:10.3389/fped.2019.00246 · Cited by 1,200 · see citing works
Self-citationMurray, C. S. (2006) · Thorax · doi:10.1136/thx.2005.042523 · Cited by 497 · see citing works
Mouse models of rhinovirus-induced disease and exacerbation of allergic airway inflammation
Bartlett, N. W., Walton, R. P., Edwards, M. R., Aniscenko, J., Caramori, G., Zhu, J., Glanville, N., Choy, K. J., Jourdan, P., Burnet, J., et al. (2008) · Nature Medicine · doi:10.1038/nm1713 · Cited by 375 · see citing works
Self-citationThe September epidemic of asthma exacerbations in children: A search for etiology
Johnston, N. W., Johnston, S. L., Duncan, J. M., Greene, J. M., Kebadze, T., Keith, P. K., Roy, M., Waserman, S., & Sears, M. R. (2005) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2004.09.025 · Cited by 343 · see citing works
Self-citationThe role of dust mites in allergy
Miller, J. D. (2019) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-018-8693-0 · Cited by 250 · see citing works
Edwards, M. R., Bartlett, N. W., Hussell, T., Openshaw, P., & Johnston, S. L. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2801 · Cited by 205 · see citing works
Self-citationPreventing severe asthma exacerbations in children. A randomized trial of mite-impermeable bedcovers
Murray, C. S., Foden, P., Sumner, H., Shepley, E., Custovic, A., & Simpson, A. (2017) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201609-1966oc · Cited by 127 · see citing works
Self-citationDel Giacco, S. R., Bakirtas, A., Bel, E., Custovic, A., Diamant, Z., Hamelmann, E., Heffler, E., Kalayci, Ö., Saglani, S., Sergejeva, S., et al. (2017) · Allergy · doi:10.1111/all.13072 · Cited by 130 · see citing works
EAACI position statement on asthma exacerbations and severe asthma
Custovic, A., Johnston, S. L., Pavord, I., Gaga, M., Fabbri, L., Bel, E. H., Le Souëf, P., Lötvall, J., Demoly, P., Akdis, C. A., et al. (2013) · Allergy · doi:10.1111/all.12275 · Cited by 127 · see citing works
Self-citationCustovic, A., & van Wijk, R. G. (2005) · Allergy · doi:10.1111/j.1398-9995.2005.00934.x · Cited by 113 · see citing works
To what extent is allergen exposure a risk factor for the development of allergic disease?
Custovic, A. (2015) · Clinical & Experimental Allergy · doi:10.1111/cea.12450 · Cited by 79 · see citing works
Edwards, M. R., Saglani, S., Schwarze, J., Skevaki, C., Smith, J. A., Ainsworth, B., Almond, M., Andreakos, E., Belvisi, M. G., Chung, K. F., et al. (2017) · European Respiratory Journal · doi:10.1183/13993003.02448-2016 · Cited by 55 · see citing works
Self-citationPediatric asthma and development of atopy
Custovic, A., Lazic, N., & Simpson, A. (2013) · Current Opinion in Allergy & Clinical Immunology · doi:10.1097/aci.0b013e32835e82b6 · Cited by 53 · see citing works
Self-citationNew treatment regimes for virus-induced exacerbations of asthma
Edwards, M. R., Kebadze, T., Johnson, M. W., & Johnston, S. L. (2006) · Pulmonary Pharmacology & Therapeutics · doi:10.1016/j.pupt.2005.09.005 · Cited by 30 · see citing works
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- Authors
- Green, R. M., Custovic, A., Sanderson, G., Hunter, J., Johnston, S. L., & Woodcock, A.
- Affiliations
- Wythenshawe Hospital (GB)
- Venue
- BMJ
- Publisher
- BMJ
- Published
- 2002-03-30
- Volume
- 324
- Issue
- 7340
- Pages
- 763
- ISSN
- 0007-1447 (ISSN-L)
- 0959-8138
- 1468-5833
- PMC
- PMC107907
- OpenAlex
- W2144836517
- Cited by
- 356
- References
- 24
- Citations by year
- 2026: 1 · 2025: 9 · 2024: 5 · 2023: 5 · 2022: 10 · 2021: 14 · 2020: 7 · 2019: 14 · 2018: 12 · 2017: 13 · 2016: 20 · 2015: 15 · 2014: 26 · 2013: 27 · 2012: 15
- FWCI
- 11.61
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.bmj.com/company/legal-information/terms-conditions/legal-information/tdm-licencepolicy (tdm)
- Locations
- BMJ (publishedVersion)
- PubMed Central (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Asthma and respiratory diseases
- Health Sciences › Medicine › Immunology and Allergy › Allergic Rhinitis and Sensitization
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Occupational exposure and asthma
- Keywords
- asthma exacerbations, hospitalization, allergen sensitization, respiratory viruses, viral infection, allergen exposure, synergistic effect, house dust mite allergens, cat allergen, dog allergen, Bla g 2, atopic status, IgE, adults
- MeSH terms
- Acute Disease, Adolescent, Adult, Allergens, Asthma, Environmental Exposure, Female, Hospitalization, Humans, Immunization, Male, Middle Aged, Risk Factors, Virus Diseases, Logistic Models, Case-Control Studies
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