Respiratory hypersensitivity reactions to NSAIDs in Europe: the global allergy and asthma network (GA2LEN) survey
Corresponding Author
J. S. Makowska
Department of Rheumatology, Medical University of Łódź, Łódź, Poland
Correspondence
Dr. Joanna Makowska, Department of Rheumatology, Medical University of Łódź, Poland.
Tel.: +48426757309
Fax: +48426782292
E-mail: [email protected]
Search for more papers by this authorP. Burney
Department of Respiratory Epidemiology and Public Health, Imperial College, London, UK
Search for more papers by this authorD. Jarvis
Department of Respiratory Epidemiology and Public Health, Imperial College, London, UK
Search for more papers by this authorT. Keil
Institute for Social Medicine, Epidemiology and Health Economics, Charité – Universitätsmedizin Berlin, Berlin, Germany
Search for more papers by this authorP. Tomassen
Upper Airways Research Laboratory, Department of Otorhinolaryngology and Logopaedic-Audiologic Science, Ghent University, Ghent, Belgium
Search for more papers by this authorJ. Bislimovska
Institute for Occupational Health of R. Macedonia, University ‘‘Sts Cyril and Methodius’’ Skopje, Skopje, Macedonia
Search for more papers by this authorG. Brozek
Department of Epidemiology, Faculty of Medicine, Medical University of Silesia, Katowice, Poland
Search for more papers by this authorC. Bachert
Upper Airways Research Laboratory, Department of Otorhinolaryngology and Logopaedic-Audiologic Science, Ghent University, Ghent, Belgium
Search for more papers by this authorJ. Baelum
Department of Occupational and Environmental Medicine, Odense University Hospital, Odense, Denmark
Search for more papers by this authorC. Bindslev-Jensen
Department of Dermatology and Allergy Centre, Odense University Hospital, Odense, Denmark
Search for more papers by this authorJ. Bousquet
Department of Respiratory Medicine, Montpellier University, Montpellier, France
Search for more papers by this authorP. J. Bousquet
Department of Respiratory Medicine, Montpellier University, Montpellier, France
Search for more papers by this authorC. Kai-Håkon
Oslo University Hospital, Rikshospitalet, Oslo, Norway
Search for more papers by this authorS. E. Dahlen
Department of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden
Search for more papers by this authorB. Dahlen
Unit of Heart and Lung Diseases, Karolinska Institutet, Stockholm, Sweden
Search for more papers by this authorW. J. Fokkens
Department of Otorhinolaryngology, Academic Medical Centre, University of Amsterdam, Amsterdam, The Netherlands
Search for more papers by this authorB. Forsberg
Department of Public Health and Clinical Medicine, Umea University, Umea, Sweden
Search for more papers by this authorM. Gjomarkaj
Department of Respiratory Medicine, Institute of Biomedicine and Molecular Immunology, Palermo, Italy
Search for more papers by this authorP. Howarth
Department of Respiratory Cell and Molecular Biology, University of Southampton, Southampton, UK
Search for more papers by this authorE. Salagean
Department of Respiratory Cell and Molecular Biology, University of Southampton, Southampton, UK
Search for more papers by this authorC. Janson
Department of Medical Sciences, Respiratory, Allergy and Sleep Research, Uppsala University, Uppsla, Sweden
Search for more papers by this authorL. Kasper
Department of Internal Medicine, Jagiellonian University Krakow, Krakow, Poland
Search for more papers by this authorU. Kraemer
Environmental Health Research Institute, Heinrich Heine University, Dusseldorf, Germany
Department of Dermatology and Allergy, Technical University Munich, Munich, Germany
Search for more papers by this authorC. Louiro
Department of Immunology and Allergology, University Hospital Coimbra, Coimbra, Portugal
Search for more papers by this authorB. Lundback
Krefting Research Centre, University of Gothenburg, Gothenburg, Sweden
Search for more papers by this authorJ. Minov
Institute for Occupational Health of R. Macedonia, University ‘‘Sts Cyril and Methodius’’ Skopje, Skopje, Macedonia
Search for more papers by this authorE. Nizankowska-Mogilnicka
Department of Internal Medicine, Jagiellonian University Krakow, Krakow, Poland
Search for more papers by this authorN. Papadopoulos
Allergy Department, 2nd Paediatric Clinic, University of Athens, Athens, Greece
Search for more papers by this authorA. G. Sakellariou
Allergy Department, 2nd Paediatric Clinic, University of Athens, Athens, Greece
Search for more papers by this authorA. Todo-Bom
Department of Immunology and Allergology, University Hospital Coimbra, Coimbra, Portugal
Search for more papers by this authorE. Toskala
Department of Otorhinolaryngology and Finnish Institute of Occupational Health, Helsinki University Hospital, Helsinki, Finland
Center for Applied Genomics, The Children's Hospital of Philadelphia, Philadelphia, PA, USA
Search for more papers by this authorJ. E. Zejda
Department of Epidemiology, Faculty of Medicine, Medical University of Silesia, Katowice, Poland
Search for more papers by this authorT. Zuberbier
Department of Dermatology and Allergy, Charite′– Universitahtsmedizin Berlin, Berlin, Germany
Search for more papers by this authorM. L. Kowalski
Department of Immunology, Rheumatology and Allergy, Medical University of Łódź, Łódź, Poland
Search for more papers by this authorCorresponding Author
J. S. Makowska
Department of Rheumatology, Medical University of Łódź, Łódź, Poland
Correspondence
Dr. Joanna Makowska, Department of Rheumatology, Medical University of Łódź, Poland.
Tel.: +48426757309
Fax: +48426782292
E-mail: [email protected]
Search for more papers by this authorP. Burney
Department of Respiratory Epidemiology and Public Health, Imperial College, London, UK
Search for more papers by this authorD. Jarvis
Department of Respiratory Epidemiology and Public Health, Imperial College, London, UK
Search for more papers by this authorT. Keil
Institute for Social Medicine, Epidemiology and Health Economics, Charité – Universitätsmedizin Berlin, Berlin, Germany
Search for more papers by this authorP. Tomassen
Upper Airways Research Laboratory, Department of Otorhinolaryngology and Logopaedic-Audiologic Science, Ghent University, Ghent, Belgium
Search for more papers by this authorJ. Bislimovska
Institute for Occupational Health of R. Macedonia, University ‘‘Sts Cyril and Methodius’’ Skopje, Skopje, Macedonia
Search for more papers by this authorG. Brozek
Department of Epidemiology, Faculty of Medicine, Medical University of Silesia, Katowice, Poland
Search for more papers by this authorC. Bachert
Upper Airways Research Laboratory, Department of Otorhinolaryngology and Logopaedic-Audiologic Science, Ghent University, Ghent, Belgium
Search for more papers by this authorJ. Baelum
Department of Occupational and Environmental Medicine, Odense University Hospital, Odense, Denmark
Search for more papers by this authorC. Bindslev-Jensen
Department of Dermatology and Allergy Centre, Odense University Hospital, Odense, Denmark
Search for more papers by this authorJ. Bousquet
Department of Respiratory Medicine, Montpellier University, Montpellier, France
Search for more papers by this authorP. J. Bousquet
Department of Respiratory Medicine, Montpellier University, Montpellier, France
Search for more papers by this authorC. Kai-Håkon
Oslo University Hospital, Rikshospitalet, Oslo, Norway
Search for more papers by this authorS. E. Dahlen
Department of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden
Search for more papers by this authorB. Dahlen
Unit of Heart and Lung Diseases, Karolinska Institutet, Stockholm, Sweden
Search for more papers by this authorW. J. Fokkens
Department of Otorhinolaryngology, Academic Medical Centre, University of Amsterdam, Amsterdam, The Netherlands
Search for more papers by this authorB. Forsberg
Department of Public Health and Clinical Medicine, Umea University, Umea, Sweden
Search for more papers by this authorM. Gjomarkaj
Department of Respiratory Medicine, Institute of Biomedicine and Molecular Immunology, Palermo, Italy
Search for more papers by this authorP. Howarth
Department of Respiratory Cell and Molecular Biology, University of Southampton, Southampton, UK
Search for more papers by this authorE. Salagean
Department of Respiratory Cell and Molecular Biology, University of Southampton, Southampton, UK
Search for more papers by this authorC. Janson
Department of Medical Sciences, Respiratory, Allergy and Sleep Research, Uppsala University, Uppsla, Sweden
Search for more papers by this authorL. Kasper
Department of Internal Medicine, Jagiellonian University Krakow, Krakow, Poland
Search for more papers by this authorU. Kraemer
Environmental Health Research Institute, Heinrich Heine University, Dusseldorf, Germany
Department of Dermatology and Allergy, Technical University Munich, Munich, Germany
Search for more papers by this authorC. Louiro
Department of Immunology and Allergology, University Hospital Coimbra, Coimbra, Portugal
Search for more papers by this authorB. Lundback
Krefting Research Centre, University of Gothenburg, Gothenburg, Sweden
Search for more papers by this authorJ. Minov
Institute for Occupational Health of R. Macedonia, University ‘‘Sts Cyril and Methodius’’ Skopje, Skopje, Macedonia
Search for more papers by this authorE. Nizankowska-Mogilnicka
Department of Internal Medicine, Jagiellonian University Krakow, Krakow, Poland
Search for more papers by this authorN. Papadopoulos
Allergy Department, 2nd Paediatric Clinic, University of Athens, Athens, Greece
Search for more papers by this authorA. G. Sakellariou
Allergy Department, 2nd Paediatric Clinic, University of Athens, Athens, Greece
Search for more papers by this authorA. Todo-Bom
Department of Immunology and Allergology, University Hospital Coimbra, Coimbra, Portugal
Search for more papers by this authorE. Toskala
Department of Otorhinolaryngology and Finnish Institute of Occupational Health, Helsinki University Hospital, Helsinki, Finland
Center for Applied Genomics, The Children's Hospital of Philadelphia, Philadelphia, PA, USA
Search for more papers by this authorJ. E. Zejda
Department of Epidemiology, Faculty of Medicine, Medical University of Silesia, Katowice, Poland
Search for more papers by this authorT. Zuberbier
Department of Dermatology and Allergy, Charite′– Universitahtsmedizin Berlin, Berlin, Germany
Search for more papers by this authorM. L. Kowalski
Department of Immunology, Rheumatology and Allergy, Medical University of Łódź, Łódź, Poland
Search for more papers by this authorAbstract
Background
Nonsteroidal anti-inflammatory drugs (NSAIDs) are among the most prevalent drugs inducing hypersensitivity reactions. The aim of this analysis was to estimate the prevalence of NSAID-induced respiratory symptoms in population across Europe and to assess its association with upper and lower respiratory tract disorders.
Methods
The GA2LEN survey was conducted in 22 centers in 15 European countries. Each of 19 centers selected random samples of 5000 adults aged 15–74 from their general population, and in three centers (Athens, Munich, Oslo), a younger population was sampled. Questionnaires including questions about age, gender, presence of symptoms of asthma, allergic rhinitis, chronic rhinosinusitis, smoking status, and history of NSAID-induced hypersensitivity reactions were sent to participants by mail. Totally, 62 737 participants completed the questionnaires.
Results
The mean prevalence of NSAID-induced dyspnea was 1.9% and was highest in the three Polish centers [Katowice (4.9%), Krakow (4.8%), and Lodz (4.4%)] and lowest in Skopje, (0.9%), Amsterdam (1.1%), and Umea (1.2%). In multivariate analysis, the prevalence of respiratory reactions to NSAIDs was higher in participants with chronic rhinosinusitis symptoms (Odds Ratio 2.12; 95%CI 1.78–2.74), asthma symptoms in last 12 months (2.7; 2.18–3.35), hospitalization due to asthma (1.53; 1.22–1.99), and adults vs children (1.53; 1.24–1.89), but was not associated with allergic rhinitis.
Conclusion
Our study documented significant variation between European countries in the prevalence of NSAID-induced respiratory hypersensitivity reactions, and association with chronic airway diseases, but also with environmental factors.
Supporting Information
Filename | Description |
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all12941-sup-0001-datas1.pdfPDF document, 438.8 KB | Data S1. GA2LEN screening questionnaire. |
all12941-sup-0001-TableS1.docxWord document, 23.2 KB | Table S1. Table GA2LEN Survey sampling frame and response rates. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- 1Ensina LF, Amigo MH, Koch T, Guzman E, Paoli R, Nunes IC. Drug hypersensitivity in students from Sao Paulo, Brazil. Clinics (Sao Paulo) 2010; 65: 1009–1011.
- 2Dona I, Blanca-Lopez N, Cornejo-Garcia JA, Torres MJ, Laguna JJ, Fernandez J et al. Characteristics of subjects experiencing hypersensitivity to non-steroidal anti-inflammatory drugs: patterns of response. Clin Exp Allergy 2011; 41: 86–95.
- 3Messaad D, Sahla H, Benahmed S, Godard P, Bousquet J, Demoly P. Drug provocation tests in patients with a history suggesting an immediate drug hypersensitivity reaction. Ann Intern Med 2004; 140: 1001–1006.
- 4Gomes E, Cardoso MF, Praca F, Gomes L, Marino E, Demoly P. Self-reported drug allergy in a general adult Portuguese population. Clin Exp Allergy 2004; 34: 1597–1601.
- 5Kowalski ML, Asero R, Bavbek S, Blanca M, Blanca-Lopez N, Bochenek G et al. Classification and practical approach to the diagnosis and management of hypersensitivity to nonsteroidal anti-inflammatory drugs. Allergy 2013; 68: 1219–1232.
- 6Kowalski ML, Makowska JS, Blanca M, Bavbek S, Bochenek G, Bousquet J et al. Hypersensitivity to nonsteroidal anti-inflammatory drugs (NSAIDs) – classification, diagnosis and management: review of the EAACI/ENDA(#) and GA2LEN/HANNA*. Allergy 2011; 66: 818–829.
- 7Demir S, Olgac M, Unal D, Gelincik A, Colakoglu B, Buyukozturk S. Evaluation of hypersensitivity reactions to nonsteroidal anti-inflammatory drugs according to the latest classification. Allergy 2015; 70: 1461–1467.
- 8Stevenson DD. Aspirin and NSAID sensitivity. Immunol Allergy Clin North Am 2004; 24: 491–505.
- 9Moon JY, Kim SH, Kim TB, Kim SH, Chang YS, Lee JH et al. Aspirin-intolerant asthma in the Korean population: prevalence and characteristics based on a questionnaire survey. Respir Med 2013; 107: 202–208.
- 10Sabry EY. The prevalence of aspirin-induced asthma in Saudian asthmatic patients. Allergol Immunopathol (Madr) 2010; 38: 181–186.
- 11Bavbek S, Yilmaz I, Celik G, Aydin O, Erkekol FO, Orman A et al. Prevalence of aspirin-exacerbated respiratory disease in patients with asthma in Turkey: a cross-sectional survey. Allergol Immunopathol (Madr) 2012; 40: 225–230.
- 12Fan Y, Feng S, Xia W, Qu L, Li X, Chen S et al. Aspirin-exacerbated respiratory disease in China: a cohort investigation and literature review. Am J Rhinol Allergy 2012; 26: e20–e22.
- 13Bavbek S, Dursun B, Dursun E, Korkmaz H, Sertkaya Karasoy D. The prevalence of aspirin hypersensitivity in patients with nasal polyposis and contributing factors. Am J Rhinol Allergy 2011; 25: 411–415.
- 14Hedman J, Kaprio J, Poussa T. Prevalence of asthma, aspirin intolerance, nasal polyposis and chronic obstructive pulmonary disease in a population-based study. Int J Epidemiol 1999; 28: 717–722.
- 15Kasper L, Sladek K, Duplaga M, Bochenek G, Liebhart J, Gladysz U et al. Prevalence of asthma with aspirin hypersensitivity in the adult population of Poland. Allergy 2003; 58: 1064–1066.
- 16Kasper L, Sladek K, Bochenek G, Duplaga M, Szczeklik A. [The frequency of hypersensitivity to non-steroidal anti-inflammatory drugs (NSAIDs) in the population of adult asthmatics in Poland based on an epidemiological questionnaire]. Pneumonol Alergol Pol 2009; 77: 431–439.
- 17Kim JE, Kountakis SE. The prevalence of Samter's triad in patients undergoing functional endoscopic sinus surgery. Ear Nose Throat J 2007; 86: 396–399.
- 18Kowalski ML, Cieslak M, Perez-Novo CA, Makowska JS, Bachert C. Clinical and immunological determinants of severe/refractory asthma (SRA): association with Staphylococcal superantigen-specific IgE antibodies. Allergy 2011; 66: 32–38.
- 19 ENFUMOSA Study Group. The ENFUMOSA cross-sectional European multicentre study of the clinical phenotype of chronic severe asthma. European network for understanding mechanisms of severe asthma. Eur Respir J 2003; 22: 470–477.
- 20Yoshimine F, Hasegawa T, Suzuki E, Terada M, Koya T, Kondoh A et al. Contribution of aspirin-intolerant asthma to near fatal asthma based on a questionnaire survey in Niigata Prefecture, Japan. Respirology 2005; 10: 477–484.
- 21Vally H, Taylor ML, Thompson PJ. The prevalence of aspirin intolerant asthma (AIA) in Australian asthmatic patients. Thorax 2002; 57: 569–574.
- 22Jarvis D, Newson R, Lotvall J, Hastan D, Tomassen P, Keil T et al. Asthma in adults and its association with chronic rhinosinusitis: the GA2LEN survey in Europe. Allergy 2012; 67: 91–98.
- 23Fokkens W, Lund V, Mullol J. European position paper on rhinosinusitis and nasal polyps. Rhinol Suppl 2007; 2007: 1–136.
- 24Settipane RA, Constantine HP, Settipane GA. Aspirin intolerance and recurrent urticaria in normal adults and children. Epidemiology and review. Allergy 1980; 35: 149–154.
- 25Jenkins C, Costello J, Hodge L. Systematic review of prevalence of aspirin induced asthma and its implications for clinical practice. BMJ 2004; 328: 434.
- 26Cavkaytar O, Arik Yilmaz E, Karaatmaca B, Buyuktiryaki B, Sackesen C, Sekerel BE et al. Different phenotypes of non-steroidal anti-inflammatory drug hypersensitivity during childhood. Int Arch Allergy Immunol 2015; 167: 211–221.
- 27 WHO database of outdoor pollution http://www.who.int/phe/health_topics/outdoorair/databases/cities/en/).
- 28Tomassen P, Jarvis D, Newson R, Van Ree R, Forsberg B, Howarth P et al. Staphylococcus aureus enterotoxin-specific IgE is associated with asthma in the general population: a GA(2)LEN study. Allergy 2013; 68: 1289–1297.
- 29 Health Fund of R. Macedonia. Annual Report 2013: Drug consumption. www.fzo.org.mk. 2006.
- 30Szczeklik A, Nizankowska E, Duplaga M. Natural history of aspirin-induced asthma. AIANE investigators. European network on aspirin-induced asthma. Eur Respir J 2000; 16: 432–436.
- 31Berges-Gimeno MP, Simon RA, Stevenson DD. The natural history and clinical characteristics of aspirin-exacerbated respiratory disease. Ann Allergy Asthma Immunol 2002; 89: 474–478.
- 32Chang JE, Ding D, Martin-Lazaro J, White A, Stevenson DD. Smoking, environmental tobacco smoke, and aspirin-exacerbated respiratory disease. Ann Allergy Asthma Immunol 2012; 108: 14–19.
- 33Viola M, Rumi G, Valluzzi RL, Gaeta F, Caruso C, Romano A. Assessing potential determinants of positive provocation tests in subjects with NSAID hypersensitivity. Clin Exp Allergy 2011; 41: 96–103.
- 34Blanca-Lopez N, Torres MJ, Dona I, Campo P, Rondon C, Seoane Reula ME et al. Value of the clinical history in the diagnosis of urticaria/angioedema induced by NSAIDs with cross-intolerance. Clin Exp Allergy 2013; 43: 85–91.