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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The influence of sensitisation to pollens and moulds on seasonal
variations in asthma attacks</title><author><name sortKey="Canova, Cristina" sort="Canova, Cristina" uniqKey="Canova C" first="Cristina" last="Canova">Cristina Canova</name><affiliation><nlm:aff id="aff1"><institution>Respiratory Epidemiology and Public Health and MRC-HPA Centre for Environment and Health, National Heart and Lung Institute, Imperial College</institution>,<addr-line>London</addr-line></nlm:aff></affiliation></author><author><name sortKey="Heinrich, Joachim" sort="Heinrich, Joachim" uniqKey="Heinrich J" first="Joachim" last="Heinrich">Joachim Heinrich</name><affiliation><nlm:aff id="aff2"><institution>Helmholtz Center Munich, German Research Center for Environmental Health</institution>,<addr-line>Neuherberg</addr-line></nlm:aff></affiliation></author><author><name sortKey="Anto, Josep Maria" sort="Anto, Josep Maria" uniqKey="Anto J" first="Josep Maria" last="Anto">Josep Maria Anto</name><affiliation><nlm:aff id="aff3"><institution>Centre for Research in Environmental Epidemiology (CREAL)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Hospital del Mar Research Institute (IMIM)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>CIBER Epidemiología y Salud Pública (CIBERESP)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff6"><institution>Dept of Life and Experimental Sciences, Universitat Pompeu Fabra</institution>,<addr-line>Barcelona</addr-line>,<country>Spain</country></nlm:aff></affiliation></author><author><name sortKey="Leynaert, Benedicte" sort="Leynaert, Benedicte" uniqKey="Leynaert B" first="Benedicte" last="Leynaert">Benedicte Leynaert</name><affiliation><nlm:aff id="aff7"><institution>National Institute of Health and Medical Research</institution>,<addr-line>INSERM Unit 700, Paris</addr-line></nlm:aff></affiliation></author><author><name sortKey="Smith, Matthew" sort="Smith, Matthew" uniqKey="Smith M" first="Matthew" last="Smith">Matthew Smith</name><affiliation><nlm:aff id="aff8"><institution>Dept of Oto-Rhino-Laryngology, Research Unit Aerobiology and Pollen Information, Medical University of Vienna</institution>,<addr-line>Vienna, Austria</addr-line></nlm:aff></affiliation></author><author><name sortKey="Kuenzli, Nino" sort="Kuenzli, Nino" uniqKey="Kuenzli N" first="Nino" last="Kuenzli">Nino Kuenzli</name><affiliation><nlm:aff id="aff9"><institution>University of Basel</institution>,<addr-line>Basel</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff10"><institution>Swiss Tropical and Public Health Institute (Swiss TPH)</institution>,<addr-line>Basel</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Zock, Jan Paul" sort="Zock, Jan Paul" uniqKey="Zock J" first="Jan-Paul" last="Zock">Jan-Paul Zock</name><affiliation><nlm:aff id="aff3"><institution>Centre for Research in Environmental Epidemiology (CREAL)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Hospital del Mar Research Institute (IMIM)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>CIBER Epidemiología y Salud Pública (CIBERESP)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation></author><author><name sortKey="Janson, Christer" sort="Janson, Christer" uniqKey="Janson C" first="Christer" last="Janson">Christer Janson</name><affiliation><nlm:aff id="aff11"><institution>Dept of Medical Sciences, Respiratory Medicine and Allergology, Uppsala University</institution>,<addr-line>Uppsala</addr-line></nlm:aff></affiliation></author><author><name sortKey="Cerveri, Isa" sort="Cerveri, Isa" uniqKey="Cerveri I" first="Isa" last="Cerveri">Isa Cerveri</name><affiliation><nlm:aff id="aff12"><institution>Clinica di Malattie dell’Apparato Respiratorio, Fondazione Ricovero e Cura a Carattere Scientifico Policlinico S. Matteo, Università di Pavia</institution>,<addr-line>Pavia</addr-line></nlm:aff></affiliation></author><author><name sortKey="De Marco, Roberto" sort="De Marco, Roberto" uniqKey="De Marco R" first="Roberto" last="De Marco">Roberto De Marco</name><affiliation><nlm:aff id="aff13"><institution>Unit of Epidemiology and Medical Statistics, Dept of Medicine and Public Health, University of Verona</institution>,<addr-line>Verona</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Toren, Kjell" sort="Toren, Kjell" uniqKey="Toren K" first="Kjell" last="Toren">Kjell Toren</name><affiliation><nlm:aff id="aff14"><institution>Section of Occupational and Environmental Medicine, Institute of Medicine, University of Gothenburg</institution>,<addr-line>Gothenburg</addr-line>,<country>Sweden</country></nlm:aff></affiliation></author><author><name sortKey="Gislason, Thorarinn" sort="Gislason, Thorarinn" uniqKey="Gislason T" first="Thorarinn" last="Gislason">Thorarinn Gislason</name><affiliation><nlm:aff id="aff15"><institution>Faculty of Medicine, University of Iceland</institution>,<addr-line>Reykjavik, Iceland</addr-line></nlm:aff></affiliation></author><author><name sortKey="Nowak, Dennis" sort="Nowak, Dennis" uniqKey="Nowak D" first="Dennis" last="Nowak">Dennis Nowak</name><affiliation><nlm:aff id="aff16"><institution>Institute and Outpatient Clinic for Occupational, Social and Environmental Medicine, Ludwig-Maximilians-University</institution>,<addr-line>Munich</addr-line></nlm:aff></affiliation></author><author><name sortKey="Pin, Isabelle" sort="Pin, Isabelle" uniqKey="Pin I" first="Isabelle" last="Pin">Isabelle Pin</name><affiliation><nlm:aff id="aff17"><institution>CHU de Grenoble, INSERM, U823, Institut Albert Bonniot, University Joseph Fourier</institution>,<addr-line>Grenoble</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Wjst, Matthias" sort="Wjst, Matthias" uniqKey="Wjst M" first="Matthias" last="Wjst">Matthias Wjst</name><affiliation><nlm:aff id="aff18"><institution>Institute of Lung Biology and Disease, CPC - Comprehensive Pneumology Center, Helmholtz Center Munich - German Research Center for Environmental Health</institution>,<addr-line>Munich</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Manfreda, Jure" sort="Manfreda, Jure" uniqKey="Manfreda J" first="Jure" last="Manfreda">Jure Manfreda</name><affiliation><nlm:aff id="aff19"><institution>Dept of Medicine, University of Manitoba</institution>,<addr-line>Winnipeg</addr-line>,<country>Canada</country></nlm:aff></affiliation></author><author><name sortKey="Svanes, Cecilie" sort="Svanes, Cecilie" uniqKey="Svanes C" first="Cecilie" last="Svanes">Cecilie Svanes</name><affiliation><nlm:aff id="aff20"><institution>Institute of Medicine, University of Bergen</institution>,<addr-line>Bergen, Norway</addr-line></nlm:aff></affiliation></author><author><name sortKey="Crane, Julian" sort="Crane, Julian" uniqKey="Crane J" first="Julian" last="Crane">Julian Crane</name><affiliation><nlm:aff id="aff21"><institution>Wellington Asthma Research Group, University of Otago</institution>,<addr-line>Wellington, New Zealand</addr-line></nlm:aff></affiliation></author><author><name sortKey="Abramson, Michael" sort="Abramson, Michael" uniqKey="Abramson M" first="Michael" last="Abramson">Michael Abramson</name><affiliation><nlm:aff id="aff22"><institution>Epidemiology and Preventive Medicine, Monash University</institution>,<addr-line>Melbourne</addr-line>,<country>Australia</country></nlm:aff></affiliation></author><author><name sortKey="Burr, Michael" sort="Burr, Michael" uniqKey="Burr M" first="Michael" last="Burr">Michael Burr</name><affiliation><nlm:aff id="aff23"><institution>Dept of Primary Care and Public Health, Cardiff University</institution>,<addr-line>Cardiff</addr-line>,<country>UK</country></nlm:aff></affiliation><affiliation></affiliation></author><author><name sortKey="Burney, Peter" sort="Burney, Peter" uniqKey="Burney P" first="Peter" last="Burney">Peter Burney</name><affiliation><nlm:aff id="aff1"><institution>Respiratory Epidemiology and Public Health and MRC-HPA Centre for Environment and Health, National Heart and Lung Institute, Imperial College</institution>,<addr-line>London</addr-line></nlm:aff></affiliation></author><author><name sortKey="Jarvis, Deborah" sort="Jarvis, Deborah" uniqKey="Jarvis D" first="Deborah" last="Jarvis">Deborah Jarvis</name><affiliation><nlm:aff id="aff1"><institution>Respiratory Epidemiology and Public Health and MRC-HPA Centre for Environment and Health, National Heart and Lung Institute, Imperial College</institution>,<addr-line>London</addr-line></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">23471350</idno><idno type="pmc">3787817</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3787817</idno><idno type="RBID">PMC:3787817</idno><idno type="doi">10.1183/09031936.00097412</idno><date when="2013">2013</date><idno type="wicri:Area/Pmc/Corpus">002473</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002473</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The influence of sensitisation to pollens and moulds on seasonal
variations in asthma attacks</title><author><name sortKey="Canova, Cristina" sort="Canova, Cristina" uniqKey="Canova C" first="Cristina" last="Canova">Cristina Canova</name><affiliation><nlm:aff id="aff1"><institution>Respiratory Epidemiology and Public Health and MRC-HPA Centre for Environment and Health, National Heart and Lung Institute, Imperial College</institution>,<addr-line>London</addr-line></nlm:aff></affiliation></author><author><name sortKey="Heinrich, Joachim" sort="Heinrich, Joachim" uniqKey="Heinrich J" first="Joachim" last="Heinrich">Joachim Heinrich</name><affiliation><nlm:aff id="aff2"><institution>Helmholtz Center Munich, German Research Center for Environmental Health</institution>,<addr-line>Neuherberg</addr-line></nlm:aff></affiliation></author><author><name sortKey="Anto, Josep Maria" sort="Anto, Josep Maria" uniqKey="Anto J" first="Josep Maria" last="Anto">Josep Maria Anto</name><affiliation><nlm:aff id="aff3"><institution>Centre for Research in Environmental Epidemiology (CREAL)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Hospital del Mar Research Institute (IMIM)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>CIBER Epidemiología y Salud Pública (CIBERESP)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff6"><institution>Dept of Life and Experimental Sciences, Universitat Pompeu Fabra</institution>,<addr-line>Barcelona</addr-line>,<country>Spain</country></nlm:aff></affiliation></author><author><name sortKey="Leynaert, Benedicte" sort="Leynaert, Benedicte" uniqKey="Leynaert B" first="Benedicte" last="Leynaert">Benedicte Leynaert</name><affiliation><nlm:aff id="aff7"><institution>National Institute of Health and Medical Research</institution>,<addr-line>INSERM Unit 700, Paris</addr-line></nlm:aff></affiliation></author><author><name sortKey="Smith, Matthew" sort="Smith, Matthew" uniqKey="Smith M" first="Matthew" last="Smith">Matthew Smith</name><affiliation><nlm:aff id="aff8"><institution>Dept of Oto-Rhino-Laryngology, Research Unit Aerobiology and Pollen Information, Medical University of Vienna</institution>,<addr-line>Vienna, Austria</addr-line></nlm:aff></affiliation></author><author><name sortKey="Kuenzli, Nino" sort="Kuenzli, Nino" uniqKey="Kuenzli N" first="Nino" last="Kuenzli">Nino Kuenzli</name><affiliation><nlm:aff id="aff9"><institution>University of Basel</institution>,<addr-line>Basel</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff10"><institution>Swiss Tropical and Public Health Institute (Swiss TPH)</institution>,<addr-line>Basel</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Zock, Jan Paul" sort="Zock, Jan Paul" uniqKey="Zock J" first="Jan-Paul" last="Zock">Jan-Paul Zock</name><affiliation><nlm:aff id="aff3"><institution>Centre for Research in Environmental Epidemiology (CREAL)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Hospital del Mar Research Institute (IMIM)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>CIBER Epidemiología y Salud Pública (CIBERESP)</institution>,<addr-line>Barcelona</addr-line></nlm:aff></affiliation></author><author><name sortKey="Janson, Christer" sort="Janson, Christer" uniqKey="Janson C" first="Christer" last="Janson">Christer Janson</name><affiliation><nlm:aff id="aff11"><institution>Dept of Medical Sciences, Respiratory Medicine and Allergology, Uppsala University</institution>,<addr-line>Uppsala</addr-line></nlm:aff></affiliation></author><author><name sortKey="Cerveri, Isa" sort="Cerveri, Isa" uniqKey="Cerveri I" first="Isa" last="Cerveri">Isa Cerveri</name><affiliation><nlm:aff id="aff12"><institution>Clinica di Malattie dell’Apparato Respiratorio, Fondazione Ricovero e Cura a Carattere Scientifico Policlinico S. Matteo, Università di Pavia</institution>,<addr-line>Pavia</addr-line></nlm:aff></affiliation></author><author><name sortKey="De Marco, Roberto" sort="De Marco, Roberto" uniqKey="De Marco R" first="Roberto" last="De Marco">Roberto De Marco</name><affiliation><nlm:aff id="aff13"><institution>Unit of Epidemiology and Medical Statistics, Dept of Medicine and Public Health, University of Verona</institution>,<addr-line>Verona</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Toren, Kjell" sort="Toren, Kjell" uniqKey="Toren K" first="Kjell" last="Toren">Kjell Toren</name><affiliation><nlm:aff id="aff14"><institution>Section of Occupational and Environmental Medicine, Institute of Medicine, University of Gothenburg</institution>,<addr-line>Gothenburg</addr-line>,<country>Sweden</country></nlm:aff></affiliation></author><author><name sortKey="Gislason, Thorarinn" sort="Gislason, Thorarinn" uniqKey="Gislason T" first="Thorarinn" last="Gislason">Thorarinn Gislason</name><affiliation><nlm:aff id="aff15"><institution>Faculty of Medicine, University of Iceland</institution>,<addr-line>Reykjavik, Iceland</addr-line></nlm:aff></affiliation></author><author><name sortKey="Nowak, Dennis" sort="Nowak, Dennis" uniqKey="Nowak D" first="Dennis" last="Nowak">Dennis Nowak</name><affiliation><nlm:aff id="aff16"><institution>Institute and Outpatient Clinic for Occupational, Social and Environmental Medicine, Ludwig-Maximilians-University</institution>,<addr-line>Munich</addr-line></nlm:aff></affiliation></author><author><name sortKey="Pin, Isabelle" sort="Pin, Isabelle" uniqKey="Pin I" first="Isabelle" last="Pin">Isabelle Pin</name><affiliation><nlm:aff id="aff17"><institution>CHU de Grenoble, INSERM, U823, Institut Albert Bonniot, University Joseph Fourier</institution>,<addr-line>Grenoble</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Wjst, Matthias" sort="Wjst, Matthias" uniqKey="Wjst M" first="Matthias" last="Wjst">Matthias Wjst</name><affiliation><nlm:aff id="aff18"><institution>Institute of Lung Biology and Disease, CPC - Comprehensive Pneumology Center, Helmholtz Center Munich - German Research Center for Environmental Health</institution>,<addr-line>Munich</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Manfreda, Jure" sort="Manfreda, Jure" uniqKey="Manfreda J" first="Jure" last="Manfreda">Jure Manfreda</name><affiliation><nlm:aff id="aff19"><institution>Dept of Medicine, University of Manitoba</institution>,<addr-line>Winnipeg</addr-line>,<country>Canada</country></nlm:aff></affiliation></author><author><name sortKey="Svanes, Cecilie" sort="Svanes, Cecilie" uniqKey="Svanes C" first="Cecilie" last="Svanes">Cecilie Svanes</name><affiliation><nlm:aff id="aff20"><institution>Institute of Medicine, University of Bergen</institution>,<addr-line>Bergen, Norway</addr-line></nlm:aff></affiliation></author><author><name sortKey="Crane, Julian" sort="Crane, Julian" uniqKey="Crane J" first="Julian" last="Crane">Julian Crane</name><affiliation><nlm:aff id="aff21"><institution>Wellington Asthma Research Group, University of Otago</institution>,<addr-line>Wellington, New Zealand</addr-line></nlm:aff></affiliation></author><author><name sortKey="Abramson, Michael" sort="Abramson, Michael" uniqKey="Abramson M" first="Michael" last="Abramson">Michael Abramson</name><affiliation><nlm:aff id="aff22"><institution>Epidemiology and Preventive Medicine, Monash University</institution>,<addr-line>Melbourne</addr-line>,<country>Australia</country></nlm:aff></affiliation></author><author><name sortKey="Burr, Michael" sort="Burr, Michael" uniqKey="Burr M" first="Michael" last="Burr">Michael Burr</name><affiliation><nlm:aff id="aff23"><institution>Dept of Primary Care and Public Health, Cardiff University</institution>,<addr-line>Cardiff</addr-line>,<country>UK</country></nlm:aff></affiliation><affiliation></affiliation></author><author><name sortKey="Burney, Peter" sort="Burney, Peter" uniqKey="Burney P" first="Peter" last="Burney">Peter Burney</name><affiliation><nlm:aff id="aff1"><institution>Respiratory Epidemiology and Public Health and MRC-HPA Centre for Environment and Health, National Heart and Lung Institute, Imperial College</institution>,<addr-line>London</addr-line></nlm:aff></affiliation></author><author><name sortKey="Jarvis, Deborah" sort="Jarvis, Deborah" uniqKey="Jarvis D" first="Deborah" last="Jarvis">Deborah Jarvis</name><affiliation><nlm:aff id="aff1"><institution>Respiratory Epidemiology and Public Health and MRC-HPA Centre for Environment and Health, National Heart and Lung Institute, Imperial College</institution>,<addr-line>London</addr-line></nlm:aff></affiliation></author></analytic><series><title level="j">The European Respiratory Journal</title><idno type="ISSN">0903-1936</idno><idno type="eISSN">1399-3003</idno><imprint><date when="2013">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>No large study has described the seasonal variation in asthma attacks in
population-based asthmatics in whom sensitisation to allergen has been
measured.</p><p>2637 young adults with asthma living in 15 countries reported the months in which
they usually had attacks of asthma and had skin-prick tests performed.
Differences in seasonal patterns by sensitisation status were assessed using
generalised estimating equations.</p><p>Most young adults with asthma reported periods of the year when their asthma
attacks were more common (range: 47% in Sweden to 86% in
Spain). Seasonal variation in asthma was not modified by sensitisation to
house dust mite or cat allergens. Asthmatics sensitised to grass, birch and
<italic>Alternaria</italic> allergens had different seasonal patterns to
those not sensitised to each allergen, with some geographical variation. In
southern Europe, those sensitised to grass allergens were more likely to report
attacks occurred in spring or summer than in winter (OR March/April 2.60,
95% CI 1.70–3.97; OR May/June 4.43, 95% CI
2.34–8.39) and smaller later peaks were observed in northern Europe
(OR May/June 1.25, 95% CI 0.60–2.64; OR July/August 1.66,
95% CI 0.89–3.10). Asthmatics reporting hay fever but who were
not sensitised to grass showed no seasonal variations.</p><p>Seasonal variations in asthma attacks in young adults are common and are
different depending on sensitisation to outdoor, but not indoor, allergens.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Hippocrates" uniqKey="Hippocrates">Hippocrates</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Khot, A" uniqKey="Khot A">A Khot</name></author><author><name sortKey="Burn, R" uniqKey="Burn R">R Burn</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fleming, Dm" uniqKey="Fleming D">DM Fleming</name></author><author><name sortKey="Cross, Kw" uniqKey="Cross K">KW Cross</name></author><author><name sortKey="Sunderland, R" uniqKey="Sunderland R">R Sunderland</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Silverman, Ra" uniqKey="Silverman R">RA Silverman</name></author><author><name sortKey="Stevenson, L" uniqKey="Stevenson L">L Stevenson</name></author><author><name sortKey="Hastings, Hm" uniqKey="Hastings 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Eur Respir J</journal-id><journal-id journal-id-type="iso-abbrev">Eur. Respir. J</journal-id><journal-id journal-id-type="publisher-id">erj</journal-id><journal-title-group><journal-title>The European Respiratory Journal</journal-title></journal-title-group><issn pub-type="ppub">0903-1936</issn><issn pub-type="epub">1399-3003</issn><publisher><publisher-name>European Respiratory Society</publisher-name><publisher-loc>442 Glossop Road, Sheffield, S10 2PX, UK</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">23471350</article-id><article-id pub-id-type="pmc">3787817</article-id><article-id pub-id-type="publisher-id">erj00974-2012</article-id><article-id pub-id-type="doi">10.1183/09031936.00097412</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject><subj-group><subject>Environmental Lung Disease</subject></subj-group></subj-group><subj-group subj-group-type="hwp-journal-coll"><subject>2</subject><subject>11</subject></subj-group></article-categories><title-group><article-title>The influence of sensitisation to pollens and moulds on seasonal
variations in asthma attacks</article-title><alt-title alt-title-type="short">Influence of pollens and moulds on seasonal asthma
variations</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Canova</surname><given-names>Cristina</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Heinrich</surname><given-names>Joachim</given-names></name><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Anto</surname><given-names>Josep Maria</given-names></name><xref ref-type="aff" rid="aff3">3</xref><xref ref-type="aff" rid="aff4">4</xref><xref ref-type="aff" rid="aff5">5</xref><xref ref-type="aff" rid="aff6">6</xref></contrib><contrib contrib-type="author"><name><surname>Leynaert</surname><given-names>Benedicte</given-names></name><xref ref-type="aff" rid="aff7">7</xref></contrib><contrib contrib-type="author"><name><surname>Smith</surname><given-names>Matthew</given-names></name><xref ref-type="aff" rid="aff8">8</xref></contrib><contrib contrib-type="author"><name><surname>Kuenzli</surname><given-names>Nino</given-names></name><xref ref-type="aff" rid="aff9">9</xref><xref ref-type="aff" rid="aff10">10</xref></contrib><contrib contrib-type="author"><name><surname>Zock</surname><given-names>Jan-Paul</given-names></name><xref ref-type="aff" rid="aff3">3</xref><xref ref-type="aff" rid="aff4">4</xref><xref ref-type="aff" rid="aff5">5</xref></contrib><contrib contrib-type="author"><name><surname>Janson</surname><given-names>Christer</given-names></name><xref ref-type="aff" rid="aff11">11</xref></contrib><contrib contrib-type="author"><name><surname>Cerveri</surname><given-names>Isa</given-names></name><xref ref-type="aff" rid="aff12">12</xref></contrib><contrib contrib-type="author"><name><surname>de Marco</surname><given-names>Roberto</given-names></name><xref ref-type="aff" rid="aff13">13</xref></contrib><contrib contrib-type="author"><name><surname>Toren</surname><given-names>Kjell</given-names></name><xref ref-type="aff" rid="aff14">14</xref></contrib><contrib contrib-type="author"><name><surname>Gislason</surname><given-names>Thorarinn</given-names></name><xref ref-type="aff" rid="aff15">15</xref></contrib><contrib contrib-type="author"><name><surname>Nowak</surname><given-names>Dennis</given-names></name><xref ref-type="aff" rid="aff16">16</xref></contrib><contrib contrib-type="author"><name><surname>Pin</surname><given-names>Isabelle</given-names></name><xref ref-type="aff" rid="aff17">17</xref></contrib><contrib contrib-type="author"><name><surname>Wjst</surname><given-names>Matthias</given-names></name><xref ref-type="aff" rid="aff18">18</xref></contrib><contrib contrib-type="author"><name><surname>Manfreda</surname><given-names>Jure</given-names></name><xref ref-type="aff" rid="aff19">19</xref></contrib><contrib contrib-type="author"><name><surname>Svanes</surname><given-names>Cecilie</given-names></name><xref ref-type="aff" rid="aff20">20</xref></contrib><contrib contrib-type="author"><name><surname>Crane</surname><given-names>Julian</given-names></name><xref ref-type="aff" rid="aff21">21</xref></contrib><contrib contrib-type="author"><name><surname>Abramson</surname><given-names>Michael</given-names></name><xref ref-type="aff" rid="aff22">22</xref></contrib><contrib contrib-type="author"><name><surname>Burr</surname><given-names>Michael</given-names></name><xref ref-type="aff" rid="aff23">23</xref><xref ref-type="aff" rid="aff24">†</xref></contrib><contrib contrib-type="author"><name><surname>Burney</surname><given-names>Peter</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Jarvis</surname><given-names>Deborah</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="corresp" rid="cor1"></xref></contrib></contrib-group><aff id="aff1"><label>1</label><institution>Respiratory Epidemiology and Public Health and MRC-HPA Centre for Environment and Health, National Heart and Lung Institute, Imperial College</institution>,<addr-line>London</addr-line></aff><aff id="aff23"><label>23</label><institution>Dept of Primary Care and Public Health, Cardiff University</institution>,<addr-line>Cardiff</addr-line>,<country>UK</country></aff><aff id="aff2"><label>2</label><institution>Helmholtz Center Munich, German Research Center for Environmental Health</institution>,<addr-line>Neuherberg</addr-line></aff><aff id="aff16"><label>16</label><institution>Institute and Outpatient Clinic for Occupational, Social and Environmental Medicine, Ludwig-Maximilians-University</institution>,<addr-line>Munich</addr-line></aff><aff id="aff18"><label>18</label><institution>Institute of Lung Biology and Disease, CPC - Comprehensive Pneumology Center, Helmholtz Center Munich - German Research Center for Environmental Health</institution>,<addr-line>Munich</addr-line>,<country>Germany</country></aff><aff id="aff3"><label>3</label><institution>Centre for Research in Environmental Epidemiology (CREAL)</institution>,<addr-line>Barcelona</addr-line></aff><aff id="aff4"><label>4</label><institution>Hospital del Mar Research Institute (IMIM)</institution>,<addr-line>Barcelona</addr-line></aff><aff id="aff5"><label>5</label><institution>CIBER Epidemiología y Salud Pública (CIBERESP)</institution>,<addr-line>Barcelona</addr-line></aff><aff id="aff6"><label>6</label><institution>Dept of Life and Experimental Sciences, Universitat Pompeu Fabra</institution>,<addr-line>Barcelona</addr-line>,<country>Spain</country></aff><aff id="aff7"><label>7</label><institution>National Institute of Health and Medical Research</institution>,<addr-line>INSERM Unit 700, Paris</addr-line></aff><aff id="aff17"><label>17</label><institution>CHU de Grenoble, INSERM, U823, Institut Albert Bonniot, University Joseph Fourier</institution>,<addr-line>Grenoble</addr-line>,<country>France</country></aff><aff id="aff8"><label>8</label><institution>Dept of Oto-Rhino-Laryngology, Research Unit Aerobiology and Pollen Information, Medical University of Vienna</institution>,<addr-line>Vienna, Austria</addr-line></aff><aff id="aff9"><label>9</label><institution>University of Basel</institution>,<addr-line>Basel</addr-line></aff><aff id="aff10"><label>10</label><institution>Swiss Tropical and Public Health Institute (Swiss TPH)</institution>,<addr-line>Basel</addr-line>,<country>Switzerland</country></aff><aff id="aff11"><label>11</label><institution>Dept of Medical Sciences, Respiratory Medicine and Allergology, Uppsala University</institution>,<addr-line>Uppsala</addr-line></aff><aff id="aff14"><label>14</label><institution>Section of Occupational and Environmental Medicine, Institute of Medicine, University of Gothenburg</institution>,<addr-line>Gothenburg</addr-line>,<country>Sweden</country></aff><aff id="aff12"><label>12</label><institution>Clinica di Malattie dell’Apparato Respiratorio, Fondazione Ricovero e Cura a Carattere Scientifico Policlinico S. Matteo, Università di Pavia</institution>,<addr-line>Pavia</addr-line></aff><aff id="aff13"><label>13</label><institution>Unit of Epidemiology and Medical Statistics, Dept of Medicine and Public Health, University of Verona</institution>,<addr-line>Verona</addr-line>,<country>Italy</country></aff><aff id="aff15"><label>15</label><institution>Faculty of Medicine, University of Iceland</institution>,<addr-line>Reykjavik, Iceland</addr-line></aff><aff id="aff19"><label>19</label><institution>Dept of Medicine, University of Manitoba</institution>,<addr-line>Winnipeg</addr-line>,<country>Canada</country></aff><aff id="aff20"><label>20</label><institution>Institute of Medicine, University of Bergen</institution>,<addr-line>Bergen, Norway</addr-line></aff><aff id="aff21"><label>21</label><institution>Wellington Asthma Research Group, University of Otago</institution>,<addr-line>Wellington, New Zealand</addr-line></aff><aff id="aff22"><label>22</label><institution>Epidemiology and Preventive Medicine, Monash University</institution>,<addr-line>Melbourne</addr-line>,<country>Australia</country></aff><aff id="aff24"></aff><author-notes><corresp id="cor1">D. Jarvis, Respiratory Epidemiology and Public Health, Imperial
College, London, Emmanuel Kaye Building, Manresa Road, London, SW3 6LR, UK.
E-mail: <email>d.jarvis@imperial.ac.uk</email></corresp></author-notes><pub-date pub-type="ppub"><month>10</month><year>2013</year></pub-date><pub-date pub-type="epub"><day>07</day><month>3</month><year>2013</year></pub-date><volume>42</volume><issue>4</issue><fpage>935</fpage><lpage>945</lpage><history><date date-type="received"><day>20</day><month>6</month><year>2012</year></date><date date-type="accepted"><day>04</day><month>1</month><year>2013</year></date></history><permissions><copyright-statement>©ERS 2013</copyright-statement><copyright-year>2013</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/"><license-p>ERJ Open articles are open access and distributed under the terms of the
(<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/">Creative
Commons Attribution Licence 3.0></ext-link>)</license-p></license></permissions><abstract><p>No large study has described the seasonal variation in asthma attacks in
population-based asthmatics in whom sensitisation to allergen has been
measured.</p><p>2637 young adults with asthma living in 15 countries reported the months in which
they usually had attacks of asthma and had skin-prick tests performed.
Differences in seasonal patterns by sensitisation status were assessed using
generalised estimating equations.</p><p>Most young adults with asthma reported periods of the year when their asthma
attacks were more common (range: 47% in Sweden to 86% in
Spain). Seasonal variation in asthma was not modified by sensitisation to
house dust mite or cat allergens. Asthmatics sensitised to grass, birch and
<italic>Alternaria</italic> allergens had different seasonal patterns to
those not sensitised to each allergen, with some geographical variation. In
southern Europe, those sensitised to grass allergens were more likely to report
attacks occurred in spring or summer than in winter (OR March/April 2.60,
95% CI 1.70–3.97; OR May/June 4.43, 95% CI
2.34–8.39) and smaller later peaks were observed in northern Europe
(OR May/June 1.25, 95% CI 0.60–2.64; OR July/August 1.66,
95% CI 0.89–3.10). Asthmatics reporting hay fever but who were
not sensitised to grass showed no seasonal variations.</p><p>Seasonal variations in asthma attacks in young adults are common and are
different depending on sensitisation to outdoor, but not indoor, allergens.</p></abstract><abstract abstract-type="short"><p><bold>Seasonal variation in asthma attacks is associated with sensitisation to
pollens and moulds, but not indoor allergens</bold><ext-link ext-link-type="uri" xlink:href="http://ow.ly/nsuRS">http://ow.ly/nsuRS</ext-link></p></abstract></article-meta></front><body><sec id="s1"><title>Introduction</title><p>As far back as the fifth century BC Hippocrates noted seasonal variation in
exacerbations of asthma [<xref ref-type="bibr" rid="b1">1</xref>]. Seasonal patterns
have been described for asthma mortality, hospital admissions and emergency
department visits [<xref ref-type="bibr" rid="b2">2</xref>–<xref ref-type="bibr" rid="b5">5</xref>], the variation being ascribed to seasonal
variation in exposure to ambient allergens, respiratory infections and
meteorological changes [<xref ref-type="bibr" rid="b4">4</xref>, <xref ref-type="bibr" rid="b6">6</xref>]. In older adults, asthma mortality and
hospital admissions are more common during the winter months (possibly
explained by infections), and in the younger adult population (a
“more atopic” generation) are more common in periods of high
ambient allergen load (grass in the spring and summer; mould in the late summer
and autumn) [<xref ref-type="bibr" rid="b7">7</xref>].</p><p>However, to date, no large study has described seasonal variation in population-based
asthmatics who also have information on IgE sensitisation. Small panel studies
suggest asthma severity is worse in the pollen season in those sensitised to grass
[<xref ref-type="bibr" rid="b8">8</xref>, <xref ref-type="bibr" rid="b9">9</xref>] and in winter in those sensitised to house dust mite [<xref ref-type="bibr" rid="b10">10</xref>]. Asthmatics presenting to accident and
emergency departments in Spain in early summer (May–June) were more
likely to be sensitised to grass than those presenting in other months [<xref ref-type="bibr" rid="b11">11</xref>]. Similarly, mild, near fatal and fatal
asthma has been associated with sensitisation to <italic>Alternaria</italic> in
months where <italic>Alternaria</italic> levels are high [<xref ref-type="bibr" rid="b12">12</xref>, <xref ref-type="bibr" rid="b13">13</xref>].</p><p>In this report we use information collected from participants in the European
Community Respiratory Health Survey (ECRHS), a large multicentre
international study of young to middle-aged adults living in differing climatic
regions and in countries with marked variation in the prevalence of sensitisation to
environmental allergens [<xref ref-type="bibr" rid="b14">14</xref>]. The aim is to
describe seasonal variation in asthma exacerbations in those who are and are not
sensitised to aeroallergens, to quantify the risk and to assess whether seasonal
patterns are consistent between countries.</p></sec><sec sec-type="materials|methods" id="s2"><title>Material and methods</title><p>The ECRHS I [<xref ref-type="bibr" rid="b15">15</xref>] recruited a random sample of
at least 3000 adults aged 20–44 years, identified from a population-based
sampling frame in each participating centre. Each was sent a postal questionnaire
and a random sample of responders plus a sample of those with symptoms suggestive of
asthma (symptomatic sample) were invited for further tests. The postal
survey, the clinical interview (at which skin-prick tests (SPTs) were
performed and blood samples taken) and the testing of samples for serum IgE
were conducted between 1991–1993.</p><p>Overall, 41 centres in 16 countries and on three continents (Europe, North
America and Australasia) followed the full protocol. Of the 24 115 participants
(random and symptomatic sample), 3353 (13.9%) reported
they “ever had asthma”. Of the participants that reported they
“ever had asthma” 3151 (94.0%) provided a complete
response to the question “Which months of the year do you usually have attacks
of asthma?” (with a response of “no” or “yes” to
each of the six bimonthly periods: January/February, March/April, May/June,
July/August, September/October and November/December). Overall, 2709
(86%) had SPTs. In one centre (Iceland), the number of
asthmatics with positive SPTs was insufficient for statistical analysis, leaving
2637 asthmatics with information on seasonality and SPTs (2023 with serum
specific IgE and total IgE measures) (online supplementary figure
S1).</p><p>SPTs to Timothy grass, <italic>Dermatophagoides pteronyssinus</italic> (house
dust mite), cat, <italic>Cladosporium herbarum</italic>, <italic>Alternaria
alternata</italic>, birch and common ragweed were performed using Phazets,
lancets precoated with standardised lyophilised allergen extracts (Pharmacia
Diagnostics AB, Uppsala, Sweden). SPTs were considered positive if the mean
wheal diameter (MWD) was >0 mm [<xref ref-type="bibr" rid="b16">16</xref>]. Serum samples were tested for specific IgE (Timothy grass,
house dust mite, cat and <italic>Cladosporium</italic> plus birch in Northern
Europe, <italic>Parietaria</italic> in Southern Europe, and ragweed in Australia and
the USA) using the Pharmacia CAP System (Pharmacia Diagnostics AB).
Sensitisation was considered present if serum IgE was >0.35
kU·L<sup>−1</sup>. Due to regulatory and ethical constraints, SPT
to Timothy grass was not performed in Germany. Ethical permission to conduct the
study was granted by local ethics committees within each participating centre.</p><sec id="s2a"><title>Statistical analysis</title><p>Each participant was considered to have taken part in six surveys: one asking if
they experienced asthma attacks in January/February, another in which they were
asked whether they experienced attacks in March/April and so on. A marginal
logistic regression model for binary outcomes, based on generalised estimating
equations, was used to generate the risk of reporting a particular 2-month
period was associated with attacks of asthma (with January/February as the
reference category). This method, which is appropriate for dealing with
longitudinal and other correlated binary response data, generates robust
estimators regardless of the specification of the covariance matrix and, as
autocorrelation is included in the covariance, coefficients can be interpreted
as usual. The bimonthly periods were shifted 6 months forward for Australian and
New Zealand centres to allow seasonal comparison across the two hemispheres.</p><p>To examine whether these patterns were different in those who were and were not
sensitised, an interaction term (positive SPT to specific allergen no/yes
× the six bimonthly periods) was included giving a total of five
interaction terms for each model. Where there was evidence of effect
modification by sensitisation, analyses were repeated stratified by
sensitisation status. Throughout, adjustments for age, sex and sensitisation to
the allergens not under assessment (four of house dust mite, grass, cat,
<italic>Alternaria</italic> and birch) were included.</p><p>Analyses were conducted within countries, but as there were insufficient data
within each country to identify patterns clearly, results from each country were
combined using meta-analytical techniques. Risk estimates for each country
within each of the three continents were combined in a random effects
meta-analysis [<xref ref-type="bibr" rid="b17">17</xref>] and heterogeneity
tested using the Q statistic and I<sup>2</sup>. As there was evidence of
heterogeneity in Europe, European countries were further divided into
central/north Europe and south Europe (defined by ±50°
latitude). As this geopolitical method of division Europe may not fully
capture pollen exposures, we also interrogated pollen maps (<ext-link ext-link-type="uri" xlink:href="www.pollenwarndienst.at">www.pollenwarndienst.at</ext-link>) to divide countries into those
with 1) Poaceae season starting before and after May or June and 2)
countries where peak birch season levels were >70.0
grains·m<sup>−3</sup> (online supplementary table
S1–2).</p><p>In sensitivity analyses, this was repeated, defining a positive SPT by MWD ≥3
mm, with sensitisation based on serum IgE measures (using both >0.35 and
>0.70 kU·L<sup>−1</sup> cut-offs), with the sample
restricted to asthmatics who reported symptoms (wheezing, chest tightness,
attack of shortness of breath coming on during the day at rest and waking with
shortness of breath) or the use of asthma medication in the last 12 months
(n=2423, 92%), and with inclusion of an adjustment for
the month of interview. Effect modification of seasonality of asthma attacks by
high total IgE (>100 kU·L<sup>−1</sup>) and reported
“hay fever or nasal allergies” was also assessed.</p><p>All analyses were undertaken in Stata IC 10.1 (Stata software version 10.1;
Stata Corp., College Station, TX, USA).</p></sec></sec><sec id="s3"><title>Results</title><p><xref ref-type="table" rid="erj-42-04-935-t01">Table 1</xref> shows the number
(range: 43 in Ireland to 387 in Canada), age and sex distributions of
participants with self-reported asthma in each country. Of these, 93%
reported “physician diagnosed asthma”. The proportion of asthmatics
sensitised to each allergen varied between countries in a pattern broadly similar to
that previously reported in the general population (<xref ref-type="table" rid="erj-42-04-935-t01">table 1</xref>) [<xref ref-type="bibr" rid="b14">14</xref>]. Allergic sensitisation to allergens associated with vegetation
(grass and birch), indoor allergens (cat and dust) and moulds
(<italic>Alternaria</italic>) was prevalent in all countries. However,
the prevalence of sensitisation to <italic>Cladosporium</italic> was low in all
countries except the USA (n=12, 18%), Canada
(n=57, 15%), Sweden (n=51, 14%) and
the UK (n=46, 13%). Similarly, the prevalence of
sensitisation to ragweed was low in most countries except Canada (n=104,
27%), the USA (n=11, 16%) and the UK
(n=16, 4%). The small number of participants precluded
inclusion of the USA in analyses of variation by these two allergens.</p><p><xref ref-type="table" rid="erj-42-04-935-t02">Table 2</xref> shows the proportion of
asthmatics who, when asked, reported their attacks of asthma usually occurred at
specific times of the year and the adjusted odds ratio of reported asthma attacks in
each bimonthly period. In most countries, most participants reported seasonal
variation in their asthma (range: 47% Sweden to 86% Spain;
median: 70% in France, Switzerland, New Zealand). In some countries,
there was no clear overall seasonal pattern (<italic>e.g.</italic> France,
Ireland, Germany and Norway), whereas in many countries
(<italic>e.g.</italic> Spain, Italy, Switzerland, Belgium, Sweden, the USA
and Australia) a significant increased risk of reported asthma attacks was seen
in the spring or summer months (March/April and May/June) compared to
winter ones. In contrast, there was an overall decreased risk of asthma in the
summer months in the Netherlands, the UK, Canada and New Zealand
(<italic>i.e.</italic> asthmatics reported their attacks of asthma usually
occurred in winter).</p><table-wrap id="erj-42-04-935-t01" position="float"><label>Table 1–</label><caption><title>Demographic characteristics and the proportion of asthmatics with
positive skin-prick test to each allergen, by country (ordered by
latitude)</title></caption><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col></colgroup><thead><tr><td align="left" rowspan="1" colspan="1"><bold>Country</bold></td><td align="center" rowspan="1" colspan="1"><bold>Subjects n</bold></td><td align="center" rowspan="1" colspan="1"><bold>Females %</bold></td><td align="center" rowspan="1" colspan="1"><bold>Age</bold></td><td align="center" rowspan="1" colspan="1"><bold>Dust mite</bold></td><td align="center" rowspan="1" colspan="1"><bold>Timothy grass</bold></td><td align="center" rowspan="1" colspan="1"><bold>Cat</bold></td><td align="center" rowspan="1" colspan="1"><bold>Birch</bold></td><td align="center" rowspan="1" colspan="1"><bold><italic>Alternaria</italic></bold></td></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1"><bold>Southern Europe</bold></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Spain</td><td align="center" rowspan="1" colspan="1">190</td><td align="center" rowspan="1" colspan="1">53</td><td align="center" rowspan="1" colspan="1">31.7±7.3</td><td align="center" rowspan="1" colspan="1">82 (43)</td><td align="center" rowspan="1" colspan="1">53 (28)</td><td align="center" rowspan="1" colspan="1">32 (17)</td><td align="center" rowspan="1" colspan="1">11 (6)</td><td align="center" rowspan="1" colspan="1">9 (5)</td></tr><tr><td align="left" rowspan="1" colspan="1"> Italy</td><td align="center" rowspan="1" colspan="1">88</td><td align="center" rowspan="1" colspan="1">52</td><td align="center" rowspan="1" colspan="1">32.9±6.9</td><td align="center" rowspan="1" colspan="1">27 (31)</td><td align="center" rowspan="1" colspan="1">41 (47)</td><td align="center" rowspan="1" colspan="1">20 (23)</td><td align="center" rowspan="1" colspan="1">19 (22)</td><td align="center" rowspan="1" colspan="1">12 (14)</td></tr><tr><td align="left" rowspan="1" colspan="1"> France</td><td align="center" rowspan="1" colspan="1">273</td><td align="center" rowspan="1" colspan="1">51</td><td align="center" rowspan="1" colspan="1">33.1±7.6</td><td align="center" rowspan="1" colspan="1">146 (53)</td><td align="center" rowspan="1" colspan="1">113 (41)</td><td align="center" rowspan="1" colspan="1">83 (30)</td><td align="center" rowspan="1" colspan="1">33 (12)</td><td align="center" rowspan="1" colspan="1">41 (15)</td></tr><tr><td align="left" rowspan="1" colspan="1"> Switzerland</td><td align="center" rowspan="1" colspan="1">122</td><td align="center" rowspan="1" colspan="1">51</td><td align="center" rowspan="1" colspan="1">31.8±6.7</td><td align="center" rowspan="1" colspan="1">37 (30)</td><td align="center" rowspan="1" colspan="1">75 (61)</td><td align="center" rowspan="1" colspan="1">37 (30)</td><td align="center" rowspan="1" colspan="1">58 (48)</td><td align="center" rowspan="1" colspan="1">11 (9)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Northern Europe</bold></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Germany</td><td align="center" rowspan="1" colspan="1">63</td><td align="center" rowspan="1" colspan="1">51</td><td align="center" rowspan="1" colspan="1">34.3±7.4</td><td align="center" rowspan="1" colspan="1">23 (37)</td><td align="center" rowspan="1" colspan="1">28<sup>#</sup> (44)</td><td align="center" rowspan="1" colspan="1">22 (35)</td><td align="center" rowspan="1" colspan="1">23 (37)</td><td align="center" rowspan="1" colspan="1">6 (10)</td></tr><tr><td align="left" rowspan="1" colspan="1"> Belgium</td><td align="center" rowspan="1" colspan="1">64</td><td align="center" rowspan="1" colspan="1">50</td><td align="center" rowspan="1" colspan="1">33.1±7.0</td><td align="center" rowspan="1" colspan="1">56 (88)</td><td align="center" rowspan="1" colspan="1">23 (36)</td><td align="center" rowspan="1" colspan="1">21 (33)</td><td align="center" rowspan="1" colspan="1">11 (17)</td><td align="center" rowspan="1" colspan="1">7 (11)</td></tr><tr><td align="left" rowspan="1" colspan="1"> The Netherlands</td><td align="center" rowspan="1" colspan="1">51</td><td align="center" rowspan="1" colspan="1">49</td><td align="center" rowspan="1" colspan="1">34.3±7.9</td><td align="center" rowspan="1" colspan="1">34 (67)</td><td align="center" rowspan="1" colspan="1">16 (31)</td><td align="center" rowspan="1" colspan="1">9 (18)</td><td align="center" rowspan="1" colspan="1">11 (22)</td><td align="center" rowspan="1" colspan="1">2 (4)</td></tr><tr><td align="left" rowspan="1" colspan="1"> Ireland</td><td align="center" rowspan="1" colspan="1">43</td><td align="center" rowspan="1" colspan="1">56</td><td align="center" rowspan="1" colspan="1">32.1±7.0</td><td align="center" rowspan="1" colspan="1">36 (84)</td><td align="center" rowspan="1" colspan="1">12 (28)</td><td align="center" rowspan="1" colspan="1">7 (16)</td><td align="center" rowspan="1" colspan="1">1 (2)</td><td align="center" rowspan="1" colspan="1">3 (7)</td></tr><tr><td align="left" rowspan="1" colspan="1"> UK</td><td align="center" rowspan="1" colspan="1">366</td><td align="center" rowspan="1" colspan="1">57</td><td align="center" rowspan="1" colspan="1">33.2±7.0</td><td align="center" rowspan="1" colspan="1">217 (59)</td><td align="center" rowspan="1" colspan="1">179 (49)</td><td align="center" rowspan="1" colspan="1">131 (36)</td><td align="center" rowspan="1" colspan="1">44 (12)</td><td align="center" rowspan="1" colspan="1">84 (23)</td></tr><tr><td align="left" rowspan="1" colspan="1"> Sweden</td><td align="center" rowspan="1" colspan="1">354</td><td align="center" rowspan="1" colspan="1">56</td><td align="center" rowspan="1" colspan="1">32.7±7.5</td><td align="center" rowspan="1" colspan="1">107 (30)</td><td align="center" rowspan="1" colspan="1">165 (47)</td><td align="center" rowspan="1" colspan="1">219 (62)</td><td align="center" rowspan="1" colspan="1">167 (47)</td><td align="center" rowspan="1" colspan="1">48 (14)</td></tr><tr><td align="left" rowspan="1" colspan="1"> Norway</td><td align="center" rowspan="1" colspan="1">60</td><td align="center" rowspan="1" colspan="1">48</td><td align="center" rowspan="1" colspan="1">33.1±6.6</td><td align="center" rowspan="1" colspan="1">13 (22)</td><td align="center" rowspan="1" colspan="1">18 (30)</td><td align="center" rowspan="1" colspan="1">16 (27)</td><td align="center" rowspan="1" colspan="1">17 (28)</td><td align="center" rowspan="1" colspan="1">2 (3)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>North America</bold></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> USA</td><td align="center" rowspan="1" colspan="1">67</td><td align="center" rowspan="1" colspan="1">49</td><td align="center" rowspan="1" colspan="1">33.6±6.8</td><td align="center" rowspan="1" colspan="1">36 (54)</td><td align="center" rowspan="1" colspan="1">31 (46)</td><td align="center" rowspan="1" colspan="1">31 (46)</td><td align="center" rowspan="1" colspan="1">18 (27)</td><td align="center" rowspan="1" colspan="1">23 (34)</td></tr><tr><td align="left" rowspan="1" colspan="1"> Canada</td><td align="center" rowspan="1" colspan="1">387</td><td align="center" rowspan="1" colspan="1">61</td><td align="center" rowspan="1" colspan="1">33.1±7.0</td><td align="center" rowspan="1" colspan="1">215 (56)</td><td align="center" rowspan="1" colspan="1">143 (37)</td><td align="center" rowspan="1" colspan="1">175 (45)</td><td align="center" rowspan="1" colspan="1">89 (23)</td><td align="center" rowspan="1" colspan="1">85 (22)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Australasia</bold></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> New Zealand</td><td align="center" rowspan="1" colspan="1">303</td><td align="center" rowspan="1" colspan="1">57</td><td align="center" rowspan="1" colspan="1">34.3±6.9</td><td align="center" rowspan="1" colspan="1">205 (68)</td><td align="center" rowspan="1" colspan="1">148 (49)</td><td align="center" rowspan="1" colspan="1">67 (22)</td><td align="center" rowspan="1" colspan="1">54 (18)</td><td align="center" rowspan="1" colspan="1">38 (13)</td></tr><tr><td align="left" rowspan="1" colspan="1"> Australia</td><td align="center" rowspan="1" colspan="1">205</td><td align="center" rowspan="1" colspan="1">53</td><td align="center" rowspan="1" colspan="1">33.6±6.8</td><td align="center" rowspan="1" colspan="1">150 (73)</td><td align="center" rowspan="1" colspan="1">111 (54)</td><td align="center" rowspan="1" colspan="1">73 (36)</td><td align="center" rowspan="1" colspan="1">19 (9)</td><td align="center" rowspan="1" colspan="1">39 (19)</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Total</bold></td><td align="center" rowspan="1" colspan="1">2637</td><td align="center" rowspan="1" colspan="1">55</td><td align="center" rowspan="1" colspan="1">33.2±7.1</td><td align="center" rowspan="1" colspan="1">1384 (53)</td><td align="center" rowspan="1" colspan="1">1128 (44)</td><td align="center" rowspan="1" colspan="1">943 (36)</td><td align="center" rowspan="1" colspan="1">575 (22)</td><td align="center" rowspan="1" colspan="1">410 (16)</td></tr></tbody></table><table-wrap-foot><fn id="nt101"><p>Data are presented as mean±<sc>sd</sc> or n (%),
unless otherwise stated. Centres: Spain (Barcelona, Galdakao,
Albacete, Oviedo and Huelva); Italy (Pavia, Turin and
Verona); France (Paris, Grenoble, Bordeaux and
Montpellier); Switzerland (Basel); Germany (Hamburg
and Erfurt); Belgium (Antwerp City and South Antwerp);
Netherlands (Groningen, Geleen and Bergen-op-zoom); Ireland
(Dublin); UK (Ipswich, Norwich, Cambridge and
Caerphilly); Sweden (Uppsala, Umea and Gothenburg);
Norway (Bergen); USA (Portland); Canada
(Winnepeg, Vancouver, Hamilton, Montreal, Halifax and Prince Edward
Island); New Zealand (Wellington, Christchurch and Hawkes
Bay); Australia (Melbourne). <sup>#</sup>: based on serum
IgE measurement.</p></fn></table-wrap-foot></table-wrap><table-wrap id="erj-42-04-935-t02" position="float"><label>Table 2–</label><caption><title>The proportion of participants with information who reported their asthma
attacks occurred at specific bimonthly periods of the year and the adjusted
odds ratio of reporting that asthma attacks usually occur in a given
bimonthly period by country<sup>#</sup></title></caption><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col><col align="center" span="1"></col></colgroup><thead><tr><td align="left" rowspan="1" colspan="1"><bold>Country</bold></td><td align="center" rowspan="1" colspan="1"><bold>Asthma attacks at specific bimonthly periods %</bold></td><td align="center" rowspan="1" colspan="1"><bold>OR Jan/Feb</bold></td><td align="center" rowspan="1" colspan="1"><bold>OR March/April</bold></td><td align="center" rowspan="1" colspan="1"><bold>OR May/June</bold></td><td align="center" rowspan="1" colspan="1"><bold>OR July/Aug</bold></td><td align="center" rowspan="1" colspan="1"><bold>OR Sept/Oct</bold></td><td align="center" rowspan="1" colspan="1"><bold>OR Nov/Dec</bold></td></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1"><bold>Spain</bold></td><td align="center" rowspan="1" colspan="1">86</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1"><bold>1.54</bold></td><td align="center" rowspan="1" colspan="1">0.94</td><td align="center" rowspan="1" colspan="1">0.47</td><td align="center" rowspan="1" colspan="1">0.90</td><td align="center" rowspan="1" colspan="1">1.11</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Italy</bold></td><td align="center" rowspan="1" colspan="1">85</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">1.54</td><td align="center" rowspan="1" colspan="1"><bold>2.44</bold></td><td align="center" rowspan="1" colspan="1">1.10</td><td align="center" rowspan="1" colspan="1">0.81</td><td align="center" rowspan="1" colspan="1">0.81</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>France</bold></td><td align="center" rowspan="1" colspan="1">70</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">0.97</td><td align="center" rowspan="1" colspan="1">1.06</td><td align="center" rowspan="1" colspan="1">0.74</td><td align="center" rowspan="1" colspan="1"><bold>0.67</bold></td><td align="center" rowspan="1" colspan="1">0.88</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Switzerland</bold></td><td align="center" rowspan="1" colspan="1">70</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1"><bold>1.74</bold></td><td align="center" rowspan="1" colspan="1"><bold>2.36</bold></td><td align="center" rowspan="1" colspan="1">1.18</td><td align="center" rowspan="1" colspan="1">1.07</td><td align="center" rowspan="1" colspan="1">0.97</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Germany</bold></td><td align="center" rowspan="1" colspan="1">76</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">1.05</td><td align="center" rowspan="1" colspan="1">1.15</td><td align="center" rowspan="1" colspan="1">0.95</td><td align="center" rowspan="1" colspan="1">1.05</td><td align="center" rowspan="1" colspan="1">1.15</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Belgium</bold></td><td align="center" rowspan="1" colspan="1">67</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">1.57</td><td align="center" rowspan="1" colspan="1"><bold>2.35</bold></td><td align="center" rowspan="1" colspan="1">1.79</td><td align="center" rowspan="1" colspan="1"><bold>2.05</bold></td><td align="center" rowspan="1" colspan="1"><bold>1.91</bold></td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>The Netherlands</bold></td><td align="center" rowspan="1" colspan="1">75</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1"><bold>0.37</bold></td><td align="center" rowspan="1" colspan="1"><bold>0.34</bold></td><td align="center" rowspan="1" colspan="1">0.85</td><td align="center" rowspan="1" colspan="1">1.09</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Ireland</bold></td><td align="center" rowspan="1" colspan="1">79</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">0.35</td><td align="center" rowspan="1" colspan="1">0.44</td><td align="center" rowspan="1" colspan="1">0.82</td><td align="center" rowspan="1" colspan="1">0.74</td><td align="center" rowspan="1" colspan="1">1.11</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>UK</bold></td><td align="center" rowspan="1" colspan="1">61</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1"><bold>0.63</bold></td><td align="center" rowspan="1" colspan="1">0.84</td><td align="center" rowspan="1" colspan="1">0.97</td><td align="center" rowspan="1" colspan="1"><bold>0.72</bold></td><td align="center" rowspan="1" colspan="1">1.00</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Sweden</bold></td><td align="center" rowspan="1" colspan="1">47</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">1.09</td><td align="center" rowspan="1" colspan="1"><bold>1.48</bold></td><td align="center" rowspan="1" colspan="1">1.04</td><td align="center" rowspan="1" colspan="1">0.91</td><td align="center" rowspan="1" colspan="1">1.09</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Norway</bold></td><td align="center" rowspan="1" colspan="1">50</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">0.86</td><td align="center" rowspan="1" colspan="1">0.74</td><td align="center" rowspan="1" colspan="1">1.18</td><td align="center" rowspan="1" colspan="1">0.86</td><td align="center" rowspan="1" colspan="1">0.74</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>USA</bold></td><td align="center" rowspan="1" colspan="1">72</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">0.83</td><td align="center" rowspan="1" colspan="1"><bold>2.38</bold></td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1">1.06</td><td align="center" rowspan="1" colspan="1">0.89</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Canada</bold></td><td align="center" rowspan="1" colspan="1">79</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1"><bold>0.70</bold></td><td align="center" rowspan="1" colspan="1">0.81</td><td align="center" rowspan="1" colspan="1">0.80</td><td align="center" rowspan="1" colspan="1">0.79</td><td align="center" rowspan="1" colspan="1">0.91</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>New Zealand<sup>¶</sup></bold></td><td align="center" rowspan="1" colspan="1">70</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1"><bold>0.71</bold></td><td align="center" rowspan="1" colspan="1"><bold>0.45</bold></td><td align="center" rowspan="1" colspan="1"><bold>0.37</bold></td><td align="center" rowspan="1" colspan="1"><bold>0.44</bold></td><td align="center" rowspan="1" colspan="1">1.00</td></tr><tr><td align="left" rowspan="1" colspan="1"><bold>Australia<sup>¶</sup></bold></td><td align="center" rowspan="1" colspan="1">59</td><td align="center" rowspan="1" colspan="1">1.00</td><td align="center" rowspan="1" colspan="1"><bold>1.66</bold></td><td align="center" rowspan="1" colspan="1">1.07</td><td align="center" rowspan="1" colspan="1">0.77</td><td align="center" rowspan="1" colspan="1">0.59</td><td align="center" rowspan="1" colspan="1">0.81</td></tr></tbody></table><table-wrap-foot><fn id="nt102"><p>Odds ratio coefficients from generalised estimating equations models
controlling for repeated individual observations, sex and age.
<sup>#</sup>: without consideration of sensitisation to
aeroallergen; <sup>¶</sup>: bimonthly periods have been shifted 6
months forward to allow comparison with the northern hemisphere.
Statistically significant results (p<0.05) are shown in
bold.</p></fn></table-wrap-foot></table-wrap><p>There was no evidence that sensitisation to house dust mite or cat allergens modified
the seasonal pattern of reported asthma attacks in any of the countries or
continents (p-value for interaction of bimonthly period by sensitisation
>0.05, I<sup>2</sup> for variation between countries <40%)
(<xref ref-type="fig" rid="erj-42-04-935-f01">fig. 1a and b</xref>).
In the few centres with sufficient data, there was some suggestion of effect
modification by having a positive SPT to ragweed (Canada, UK) throughout
the summer and early autumn (p<0.05 only in September/October) and by
having a positive SPT to <italic>Cladosporium</italic> in July/August (UK,
Sweden and Canada) but formal testing showed this to be below the conventional
limits of statistical significance (<xref ref-type="fig" rid="erj-42-04-935-f01">fig. 1c and d</xref>).</p><fig id="erj-42-04-935-f01" position="float"><label>Figure 1–</label><caption><p>The overall adjusted odds ratio (error bars represent 95%
confidence intervals) of asthma usually occurring in each bimonthly
period in those sensitised to a) house dust mite in all countries;
b) cat in all countries; c) <italic>Cladosporium</italic> in
Sweden, the UK and Canada; and d) ragweed in the UK and Canada. Overall
adjusted odds ratios are from meta-analysis of interaction coefficients from
generalised estimating equations models conducted within country controlling
for repeated individual observations, main effect of relevant allergen and
bimonthly periods, sex, age and sensitisation to dust mite (for
cat), cat (for house dust mite) and grass, birch and
<italic>Alternaria.</italic> j/f: January/February; m/a: March/April;
m/j: May/June; j/a: July/August; s/o: September/October; n/d:
November/December.</p></caption><graphic xlink:href="erj-42-04-935-f01"></graphic></fig><p>In contrast, there was evidence that seasonal variation was modified by sensitisation
to grass, birch and <italic>Alternaria</italic> (online supplementary figures
S2–S4 show meta-analysis of the interaction coefficients). In <xref ref-type="fig" rid="erj-42-04-935-f02">figures 2</xref>–<xref ref-type="fig" rid="erj-42-04-935-f04">4</xref>, the odds of reporting asthma
attacks in each bimonthly period are shown, stratified by sensitisation status.
There was considerable variation in Europe (for example, I<sup>2</sup> for the
interaction terms for grass in May/June and birch sensitisation in March/April
within Europe were 61% and 76%, respectively). When Europe was
considered as north and south, or divided based on available average pollen levels
over the past 15 years (early/late Poaceae season or by peak birch pollen
levels reached) some differences still remained.</p><fig id="erj-42-04-935-f02" position="float"><label>Figure 2–</label><caption><p>The overall adjusted odds ratio (error bars represent 95%
confidence intervals) of asthma usually occurring in each bimonthly
period in those sensitised to grass and in those not sensitised to grass in
a) south Europe; b) north Europe; c) North America; and
d) Australasia (bimonthly periods have been shifted 6 months
forward to allow comparison with the northern hemisphere). Overall
adjusted odds ratios are from meta-analysis of bimonthly period coefficients
from generalised estimating equations models conducted within country
controlling for repeated individual observations, sex, age and sensitisation
to dust, cat, <italic>Alternaria</italic> and birch. j/f: January/February;
m/a: March/April; m/j: May/June; j/a: July/August; s/o: September/October;
n/d: November/December. <sup>#</sup>: p-heterogeneity <0.05; *:
p-value for interaction <0.05.</p></caption><graphic xlink:href="erj-42-04-935-f02"></graphic></fig><fig id="erj-42-04-935-f03" position="float"><label>Figure 3–</label><caption><p>The overall adjusted odds ratio (error bars represent 95%
confidence intervals) of asthma usually occurring in each bimonthly
period in those with reported hay fever sensitised and not sensitised to
grass in a) south Europe; b) north Europe; c) North America;
and d) Australasia (bimonthly periods have been shifted 6 months
forward to allow comparison with the northern hemisphere). Overall
adjusted odds ratios are from meta-analysis of bimonthly period coefficients
from generalised estimating equations models conducted within country
controlling for repeated individual observations, sex, age (only among
subjects with sensitisation to dust, cat, <italic>Alternaria</italic> and
birch data). j/f: January/February; m/a: March/April; m/j: May/June;
j/a: July/August; s/o: September/October; n/d: November/December.
<sup>#</sup>: p-heterogeneity <0.05.</p></caption><graphic xlink:href="erj-42-04-935-f03"></graphic></fig><fig id="erj-42-04-935-f04" position="float"><label>Figure 4–</label><caption><p>The overall adjusted odds ratio (error bars represent 95%
confidence intervals) of asthma usually occurring in each bimonthly
period in those sensitised to birch and in those not sensitised to birch in
a) south Europe; b) north Europe (the Netherlands and Ireland
were not included due to few asthmatics sensitised to birch producing a lack
of model convergence); c) North America; and d) Australasia
(bimonthly periods have been shifted 6 months forward to allow
comparison with the northern hemisphere). Overall adjusted odds ratios
are from meta-analysis of bimonthly periods coefficients from generalised
estimating equations models conducted within country controlling for
repeated individual observations, sex, age and sensitisation to grass, dust,
cat and <italic>Alternaria.</italic> j/f: January/February; m/a:
March/April; m/j: May/June; j/a: July/August; s/o: September/October; n/d:
November/December. <sup>#</sup>: p-heterogeneity <0.05; *: p-value
for interaction <0.05.</p></caption><graphic xlink:href="erj-42-04-935-f04"></graphic></fig><p>In both south and north Europe (<xref ref-type="fig" rid="erj-42-04-935-f02">fig. 2a and b</xref>), those sensitised to grass were more likely to
report that their asthma attacks usually occur in the spring/summer periods than in
the winter period, while those who were not sensitised were more likely to report
attacks in the winter months. For those who were grass sensitised, the higher risks
were in early summer in southern Europe (OR March/April 2.60, 95% CI
1.70–3.97; OR May/June 4.43, 95% CI 2.34–8.39), and by
comparison, in northern Europe the peak risks were relatively smaller, occurred
later and showed more variation between the countries (OR July/August 1.66,
95% CI 0.89–3.10; I<sup>2</sup> 61%). Similar patterns were
seen in Europe when countries were considered to have an early or late grass pollen
season (online supplementary fig. S5). In North America (<xref ref-type="fig" rid="erj-42-04-935-f02">fig. 2c</xref>), the pattern was
similar to that seen for southern Europe (although all interaction terms
p>0.05). In Australia and New Zealand (<xref ref-type="fig" rid="erj-42-04-935-f02">fig. 2d</xref>), the effect of grass sensitisation
on asthma attacks was more complex, being different in the two countries, and
superimposed on an overall decreased risk of attacks during the summer or autumn
months. Formal testing for modification of the seasonal pattern by sensitisation to
grass was significant (p<0.05) only in March/April. In all regions, the
seasonal pattern of asthma amongst those reporting “hay fever or nasal
allergies” (overall, 77% of asthmatics also reported hay
fever) was similar to that seen for grass sensitisation (54% of
those with hay fever also had sensitisation to grass) (online
supplementary fig. S5). However, this pattern was only present in those
sensitised to grass, and not seen in those who reported hay fever but who were not
sensitised to grass (<xref ref-type="fig" rid="erj-42-04-935-f03">fig.
3</xref>).</p><p>In Europe, asthmatics who were sensitised to birch were more likely to report that
their attacks occurred in the spring or summer than in the winter months. The
seasonal pattern amongst those who were sensitised to birch was clearly seen in
northern Europe (OR May/June 2.94, 95% CI 1.92–4.50; OR
July/August 2.01, 95% CI 1.38–2.94) (<xref ref-type="fig" rid="erj-42-04-935-f04">fig. 4b</xref>), although there was some variation
between countries (<italic>e.g.</italic> OR May/June 0.87, 95% CI
0.55–1.37; I<sup>2</sup>: 72%). The pattern was seen in countries
where peak birch pollen levels exceeded 70.0 grains·m<sup>−3</sup>(online supplementary fig. S6), but again there was some variation in the
magnitude of the effect between countries. Compared to grass sensitisation, the peak
risk in this sensitised group occurred earlier in the year (<xref ref-type="fig" rid="erj-42-04-935-f03">fig 3b</xref> and <xref ref-type="fig" rid="erj-42-04-935-f04">fig. 4b</xref>]). Some seasonal variation was also
seen in southern Europe (where birch pollen levels are generally lower).
There was no evidence that sensitisation to birch modified seasonal variation of
asthma attacks in North America or Australasia (all interactions p>0.05;
<xref ref-type="fig" rid="erj-42-04-935-f04">fig. 4c–d</xref>).</p><p>Asthmatics who were sensitised to <italic>Alternaria</italic> were at a greater risk
of reporting asthma attacks in May/June and July/August in southern Europe
(<xref ref-type="fig" rid="erj-42-04-935-f05">fig. 5a</xref>) and in
July/August in north Europe (<xref ref-type="fig" rid="erj-42-04-935-f05">fig.
5b</xref>). There was some evidence of similar seasonal patterns of
reporting asthma attacks in North America (<xref ref-type="fig" rid="erj-42-04-935-f05">fig. 5c</xref>) (formal testing for
interactions p<0.05 in July/August) and in Australasia (<xref ref-type="fig" rid="erj-42-04-935-f05">fig. 5d</xref>) the pattern was
similar to that seen for grass sensitisation.</p><fig id="erj-42-04-935-f05" position="float"><label>Figure 5–</label><caption><p>The overall adjusted odds ratio (error bars represent 95%
confidence intervals) of asthma usually occurring in each bimonthly
period in those sensitised to <italic>Alternaria</italic> and in those not
sensitised to <italic>Alternaria</italic> in a) south Europe; b)
north Europe (the Netherlands, Belgium, Ireland and Norway were not
included due to few asthmatics sensitised to <italic>Alternaria</italic>producing a lack of model convergence); c) North America; and
d) Australasia (bimonthly periods have been shifted 6 months
forward to allow comparison with the northern hemisphere). Overall
adjusted odds ratios are from meta-analysis of bimonthly periods
coefficients from generalised estimating equations models conducted within
country controlling for repeated individual observations, sex, age and
sensitisation to grass, dust, cat and birch. j/f: January/February; m/a:
March/April; m/j: May/June; j/a: July/August; s/o: September/October; n/d:
November/December. <sup>#</sup>: p-heterogeneity <0.05; *: p-value
for interaction <0.05.</p></caption><graphic xlink:href="erj-42-04-935-f05"></graphic></fig><p>None of the above observations were substantially altered by changing the definition
of a positive SPT (MWD ≥3 mm), by using serum specific IgE to define
sensitisation (using a cut off of 0.35 or 0.70
kU·L<sup>−1</sup>), by restricting the sample to those who had
asthma symptoms in the past year or by including the month of interview (and
SPT) as a potential confounder. Furthermore, high levels of total IgE
(>100 kU·mL<sup>−1</sup>) did not influence seasonal
variations (data not shown).</p></sec><sec id="s4"><title>Discussion</title><p>This large study of >2500 young adults with asthma shows that a substantial
proportion report seasonal variation in their attacks of asthma, and that the
pattern of the seasonal variation is dependent on whether they are sensitised to
pollens and moulds, but not indoor allergens. Asthmatics sensitised to grass, birch
and <italic>Alternaria</italic> show very different seasonal patterns to those not
sensitised to these allergens. This is most clearly seen for sensitisation to grass,
where individuals who are sensitised report more attacks in the summer months
(most likely related to allergen exposure) and those who are not
sensitised report more attacks in the winter months (most likely due to the
effects of respiratory infections [<xref ref-type="bibr" rid="b6">6</xref>]).
Although these patterns are widely recognised by clinicians, to date, no
epidemiological study of this scale has described these patterns, or derived risk
estimates associated with sensitisation status in representative samples of the
asthmatic population.</p><p>Beyond the clear relevance for clinical practice, our results provide important
baseline information for risk assessment in relation to climate change and may
assist in the interpretation of health effects of outdoor air pollution on
asthma.</p><p>We would expect the seasonal pattern in those who are sensitised to pollens and mould
to mirror the patterns of exposure. We do not have complete information on pollen
levels in all of our participating centres for the period of data collection
(1991–1992). Two groups (the European Academy of Allergy and
Clinical Immunology and the International Association of Aerobiology) collated
all available pollen data from Europe (1974–1988) [<xref ref-type="bibr" rid="b18">18</xref>], which showed peak grass
(Poaceae) pollen counts occurred later in northern than southern Europe,
and in some countries (<italic>e.g.</italic> northern Italy) were raised
well into September/October. In Scandinavian countries, the birch pollen season
began in May, lasting at least until the end of August, while the season was
earlier, shorter and more intense in “southern” Europe. The
“average” pollen season over the last 15 years is broadly similar to
these patterns (<ext-link ext-link-type="uri" xlink:href="www.pollenwarndienst.at">www.pollenwarndienst.at</ext-link>)
and more recent European work confirms these temporal and geographical variations in
grass pollen [<xref ref-type="bibr" rid="b19">19</xref>, <xref ref-type="bibr" rid="b20">20</xref>], birch [<xref ref-type="bibr" rid="b21">21</xref>] and
mould spore counts (<italic>Alternaria</italic> and
<italic>Cladosporium</italic>) [<xref ref-type="bibr" rid="b22">22</xref>,
<xref ref-type="bibr" rid="b23">23</xref>]. However, there is growing evidence
that measurement of pollen allergenicity (a subject of research within
multicentre initiatives such as the Health Impacts of Airborne Allergen Information
Network; <ext-link ext-link-type="uri" xlink:href="www.hialine.com">www.hialine.com</ext-link>), rather than pollen counts, may be the
relevant exposure to explain allergen associated variations in asthma exacerbations
[<xref ref-type="bibr" rid="b24">24</xref>].</p><p>Our report suggests that mortality and admissions are the “tip of the
iceberg” of seasonal variations in asthma. Most asthma treatment guidelines
list exposure to seasonal allergens as a potential trigger to asthma attacks [<xref ref-type="bibr" rid="b25">25</xref>], and our data support that those with
sensitisation to grass, birch and <italic>Alternaria</italic> (and possibly
<italic>Cladosporium</italic>) may benefit from focussed clinical protocols
[<xref ref-type="bibr" rid="b26">26</xref>] that increase inhaled treatment
during the months of peak exposure to allergen. They may even benefit from
desensitisation and immunotherapy (2.6% of asthmatics reported they
“had been vaccinated for allergy in the previous 12 months”).
Assessment of sensitisation by SPTs and/or serum measures may not be routinely
performed in all primary healthcare settings. However, the interpretation of such
testing requires understanding of potential cross-reactivity and should be carefully
considered alongside information on likely exposure. For example, some people may
test positive to ragweed in the UK, but ragweed pollen is absent there.
Sensitisation probably arises from cross-reactivity with other members of the
Compositae (Asteraceae) family (<italic>e.g.</italic> mugwort).
Even though our data suggest that people with positive SPTs to ragweed in the UK and
Canada have different seasonal patterns, particularly in late summer, compared to
those without positive SPTs (<xref ref-type="fig" rid="erj-42-04-935-f01">fig.
1d</xref>), this might be explained by residual confounding by mould
exposure. Similarly, the pattern of variation that we have seen in those who do and
do not have positive SPTs to birch in southern Europe may in part be explained by
cross-reactivity with other members of the Bet v 1-family
(<italic>e.g.</italic> hazel and hop-hornbeam) [<xref ref-type="bibr" rid="b27">27</xref>]. Asthmatics who also reported hay fever showed an increased
risk of reporting exacerbations in the spring and summer months but this was limited
to those who were grass sensitised. Although reporting hay fever identifies those at
greater risk of spring/summer asthma exacerbations (online supplementary fig.
E7), the addition of testing for grass sensitisation may be more useful to
identify those at risk (<xref ref-type="fig" rid="erj-42-04-935-f03">fig.
3</xref>). Indoor allergens, such as house dust mite and cat, may have a
role in determining asthma exacerbations and severity of disease, but our data
suggest that those sensitised to indoor allergens have the same seasonal variations
as those who are not sensitised to these allergens.</p><p>Large time series and ecological studies of asthma mortality and admissions in
relation to pollen or mould exposure [<xref ref-type="bibr" rid="b7">7</xref>, <xref ref-type="bibr" rid="b28">28</xref>–<xref ref-type="bibr" rid="b32">32</xref>] present effect estimates for the entire population and have not
included differences in effect in those who are and are not sensitised (the
proportion of which varies between countries). The effect of pollen on
sensitised individuals may confound the respiratory effects of other outdoor
pollutants, particularly ozone (which peaks during the summer months).
This could explain the inconsistency in the association of ozone with asthma
reported in some time series studies [<xref ref-type="bibr" rid="b33">33</xref>,
<xref ref-type="bibr" rid="b34">34</xref>]. Possible interactions between air
pollutants and aeroallergens and their effect on asthma exacerbations have been
investigated in few studies. Individual sensitisation to such aeroallergens might
influence the observed effects and explain why such interactions are only seen in
some studies [<xref ref-type="bibr" rid="b35">35</xref>].</p><p>Climate change may lead to more intense and extended pollen or mould seasons with
higher absolute levels and increased allergenicity [<xref ref-type="bibr" rid="b36">36</xref>, <xref ref-type="bibr" rid="b37">37</xref>]. There may be more
thunderstorms, which are known to cause sudden peaks in grass and mould allergen
levels and “epidemic asthma” in those who are sensitised [<xref ref-type="bibr" rid="b11">11</xref>, <xref ref-type="bibr" rid="b38">38</xref>].
This report provides baseline information showing that those who are sensitised are
indeed a subgroup of the population who will be particularly at risk if these
climatic changes occur.</p><p>The ideal study design to investigate the effects of pollen exposure on asthma
exacerbations is a longitudinal or panel study of asthmatics who provide symptom and
sensitisation information at regular intervals over a 1-year period, but only one
large study of this type (on children) has been reported [<xref ref-type="bibr" rid="b39">39</xref>]. Although our study design is not optimal,
it is, to our knowledge, the only large international study of seasonal variations
in population-based asthmatics in whom atopic status has been assessed. Participants
were identified from representative community based samples (not from hospital
clinics) and even though the vast majority reported a physician diagnosis of
asthma, only a third reported using inhaled steroids in the past year
(reflecting that they had relatively mild disease [<xref ref-type="bibr" rid="b40">40</xref>] and the under-treatment of asthma during the 1990s).
We have relied on self-reported seasonality collected at one point in time, which
has high face validity but may introduce random error (making it more difficult
to identify clear patterns). Systematic error is unlikely as seasonal reporting
was not influenced by month of interview or by participants knowing their IgE status
(questionnaire was asked before SPT).</p><p>Even though our report is based on observations made 20 years ago, similar patterns
were still seen in adults who took part in ECRHS II (a subsample of
participants included in this report who were followed up in 2000–2002,
n=1284, aged 27–54 years at follow-up, 12 countries) who underwent
repeat questionnaires and limited serum IgE testing (no SPTs were performed in
ECRHS II) (online supplementary fig. E8).</p><p>We have described geographical variation in seasonality but, because of the
relatively small sample size in some centres, have grouped information from centres
to country level, and then regional level. Our regions are thus defined by
geopolitics rather than factors that others may consider more relevant
(<italic>e.g.</italic> pollen levels, climate and land usage).</p><p>In conclusion, we have shown that seasonal variation in asthma attacks in young
adults is common and is strongly associated with allergic sensitisation. This is a
timely reminder to clinicians to remain alert to seasonal allergens as a potential
trigger for asthma attacks in their sensitised patients. Air pollution scientists
should strive to include measures of allergen exposure and measures of individual
(or at least population levels) of allergic sensitisation in their
analyses. Climate change may increase pollen levels and their allergenicity, and
also extend pollen seasons; this will probably lead to increased exacerbations in
those who are sensitised to these aeroallergens. Large panel studies to better
understand and quantify the relationships between exacerbations, allergic
sensitisation, directly measured pollen counts and other factors are required.</p></sec></body><back><ack><p>This paper is dedicated to the memory of Dr Michael (“Mike”)
Burr.</p></ack><fn-group><fn fn-type="supplementary-material"><p>For editorial comments see <related-article related-article-type="commentary" id="d35e3430" vol="42" page="898" ext-link-type="pmc">page
898</related-article>.</p></fn><fn fn-type="supplementary-material"><p>This article has supplementary material available from <ext-link ext-link-type="uri" xlink:href="www.erj.ersjournals.com">www.erj.ersjournals.com</ext-link></p></fn><fn fn-type="financial-disclosure"><p>Support statement: Co-ordination of the ECRHS I was supported by a grant from the
<funding-source>European Commission</funding-source>. Skin-prick testing with
Phazet received grant support from Pharmacia Diagnostics (Uppsala,
Sweden). Each local centre was funded by local funding agencies
(described in the online supplementary material). C. Canova is funded
by the <funding-source>Medical Research Council</funding-source> and
<funding-source>Health Protection Agency</funding-source>(G0801056).</p></fn><fn fn-type="conflict"><p>Conflict of interest: Disclosures can be found alongside the online version of
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