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Who's at risk of thunderstorm asthma? The ryegrass pollen trifecta and lessons learnt from the Melbourne thunderstorm epidemic

  • Joy Lee
    Correspondence
    Corresponding author. Present address: Allergy, Asthma & Immunology, The Alfred Hospital, 55 Commercial Road, Melbourne, VIC, 3004, Australia.
    Affiliations
    Allergy, Asthma & Clinical Immunology, The Alfred Hospital, Melbourne, Australia

    School of Public Health & Preventive Medicine, Monash University, Melbourne, Australia
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  • Caroline Kronborg
    Affiliations
    Allergy, Asthma & Clinical Immunology, The Alfred Hospital, Melbourne, Australia
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  • Robyn E. O'Hehir
    Affiliations
    Allergy, Asthma & Clinical Immunology, The Alfred Hospital, Melbourne, Australia

    Allergy, Immunology & Respiratory Medicine, Central Clinical School, Monash University, Melbourne, Australia
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  • Mark Hew
    Affiliations
    Allergy, Asthma & Clinical Immunology, The Alfred Hospital, Melbourne, Australia

    School of Public Health & Preventive Medicine, Monash University, Melbourne, Australia
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Open ArchivePublished:October 17, 2017DOI:https://doi.org/10.1016/j.rmed.2017.10.012

      Highlights

      • Ryegrass pollen sensitizsation, allergic rhinitis and allergen exposure are a risk ‘trifecta’ for thunderstorm asthma.
      • In contrast, the majority (60%) of patients presenting with thunderstorm asthma did not have a prior diagnosis of asthma.
      • The development of public health measures to target these identified key risk factors are essential to mitigate future risk.

      Abstract

      The Melbourne thunderstorm asthma epidemic in November 2016 was unprecedented in scale and impact. We systematically reviewed our hospital's patients with thunderstorm asthma to identify key risk factors. Of 85 adult patients assessed, the majority (60%) had no prior diagnosis of asthma. However, allergic rhinitis during the grass pollen season was almost universal (99%), as were ryegrass pollen sensitization (100%) and exposure to the outdoor environment during the thunderstorm (94%). Airborne pollen levels on the thunderstorm day were extreme. We conclude that ryegrass pollen sensitization, clinical allergic rhinitis, and acute allergen exposure constitute a risk-factor ‘trifecta’ for thunderstorm asthma.

      Graphical abstract

      Keywords

      Abbreviations:

      CI (Confidence Interval), FEV1 (Forced expiratory volume during the first second), FVC (Forced vital capacity), FER (Forced expiratory ratio), IgE (immunoglobulin E), SD (Standard deviation), SPT (skin prick test), RAST (Radioallergosorbent test)

      1. Introduction

      Thunderstorms have triggered sudden asthma epidemics throughout the world [
      • D'Amato G.
      • Vitale C.
      • D'Amato M.
      • Cecchi L.
      • Liccardi G.
      • Molino A.
      • et al.
      Thunderstorm-related asthma: what happens and why.
      ]. The evidence mostly suggests an allergic aetiology due to plant pollens and fungal spores [
      • D'Amato G.
      • Vitale C.
      • D'Amato M.
      • Cecchi L.
      • Liccardi G.
      • Molino A.
      • et al.
      Thunderstorm-related asthma: what happens and why.
      ]. Importantly, thunderstorm asthma can affect individuals without prior asthma [
      • Girgis S.T.
      • Marks G.B.
      • Downs S.H.
      • Kolbe A.
      • Car G.N.
      • Paton R.
      Thunderstorm-associated asthma in an inland town in south-eastern Australia. Who is at risk?.
      ]. This unpredictable element hinders effective targeting of protective measures for thunderstorm asthma.
      On the 21st of November 2016 at 1700 h, a springtime thunderstorm struck Melbourne, Australia, and triggered the most devastating thunderstorm asthma epidemic to date [
      • Hew M.
      • Sutherland M.
      • Thien F.
      • O'Hehir R.
      The Melbourne thunderstorm asthma event: can we avert another strike?.
      ]. In a city of nearly five million, ambulances and emergency departments were overwhelmed by 3500 presentations, with many times that number treated urgently in the community [

      State of Victoria. Review of response to the thunderstorm asthma event of 21–22 November 2016 Port Melbourne: Department of Justice and Regulation, 2017 27 April Report No.: 978-1-925549-31-7.

      ]. Thirty-five patients required intensive care admission, and nine deaths are under coronial investigation.
      We systematically examined our cohort of patients at Alfred Health, Melbourne, to identify key susceptibility factors.

      2. Methods

      We reviewed records of all patients aged ≥16 years with symptoms suggestive of asthma (dyspnoea, respiratory distress, cough or wheeze) presenting to the emergency departments of Alfred Health between 1700 h 21st November, and 1700 h, 23rd November 2016. For patients discharged from Emergency, we attempted repeated telephone contact to offer review at our specialist asthma and allergy clinic. All patients admitted with thunderstorm asthma were scheduled for review.
      A detailed asthma history was obtained. On spirometry, an obstructive ventilatory defect was defined by an FEV1/FVC ratio below the lower limit of normal (for age, weight and height). A significant bronchodilator response was defined as an increase in FEV1 by ≥ 12% AND ≥200 ml following bronchodilator.
      We defined ‘seasonal allergic rhinitis’ as the presence of rhinitis symptoms during Melbourne's spring (September to November); ‘perennial allergic rhinitis’ as perennial symptoms at a similar intensity; and ‘perennial rhinitis with seasonal exacerbation’ as perennial symptoms with at least fifty percent worsening during Melbourne's spring.
      Patients were designated atopic if they had at least one wheal ≥3 mm on skin prick to twenty aeroallergens (Stallergenes-Greer®, Antony, France) or a serum allergen-specific IgE >0.34kUA/L (ImmunoCap® Abacus ALS, Brisbane, Australia) to at least one of: Ryegrass pollen, Bermuda grass pollen, Alternaria and Cladosporium. During the thunderstorm, Ryegrass was in pollination. Cladosporium and Alternaria fungal spores have previously been detected in the atmosphere during the season.
      Patients were asked their location before and during the thunderstorm (between 1700 and 2000 h). The pollen count was obtained from ‘Melbourne Pollen Count’ (http://www.melbournepollen.com.au/index.php/forecast).
      Ethics approval was obtained (Alfred ref. 20/17). Data analysis was performed using SPSS version 22 (IBM, Armonk, NY). Categorical variables are presented as percentages (frequency) and continuous variables as mean values with standard deviation.

      3. Results

      From 1188 emergency records, 243 patients had asthma symptoms. Of these, 168/243 (68%) were contactable, but 37 declined appointments. Of 131 scheduled appointments, 15 patients cancelled and 29 failed to attend; 87 attended clinic between 22nd December 2016 and 1st June 2017, at which two were found not to have thunderstorm asthma. Eighty-five clinic patients with thunderstorm asthma are described in Table 1.
      Table 1Baseline demographics.
      Demographicsn = 85
      Age, mean (range, SD) years4016-81, 16
      Gender, n (%) Male5160%
      Smoking status, n (%)
      Never5362%
      Ex-smoker2732%
      Current56%
      Disposition from Emergency department
      Home7285%
      Short stay unit or general ward1113%
      Intensive care22%
      Asthma history
      No previous asthma3035%
      Undiagnosed asthma2125%
      Known asthma3440%
      n = 34
      Current asthma1956%
      Childhood asthma1132%
      Previous thunderstorm asthma (November 2010)412%
      Allergic Rhinitis
      Symptoms during ryegrass pollen season (September-November)8499%
      Seasonal allergic rhinitis only7588%
      Perennial allergic rhinitis with seasonal exacerbation67%
      Perennial rhinitis without seasonal exacerbation34%
      Allergic rhinitis clinical severity
      Mild2631%
      Moderate4250%
      Severe1619%
      Allergic Sensitization
      Serum (n = 68)
      Ryegrass68100%
      Bermuda grass6394%
      Alternaria57%
      Cladosporium34%
      Skin prick test (n = 75)
      Ryegrass7397%
      Timothy grass6891%
      Plantain grass4965%
      Bahia grass7095%
      Ragweed4966%
      Cypress tree3547%
      Wattle tree3344%
      Birch tree3344%
      Plane tree2736%
      Cat dander2736%
      Dog dander1115%
      Horse dander912%
      House dust mite (D. pteronyssinus)5067%
      Alternaria912%
      Cladosporium45%
      Aspergillus67%
      Penicillium11%
      Trichophyton811%
      Outdoors exposure during thunderstorm
      Exposed8094%
      Physically outdoors5771%
      Indoors with open windows2329%
      Not exposed56%
      Abbreviations: n = number, SD = standard deviation, IgE = immunoglobulin E.
      Of nineteen patients with known current asthma, nine had an inhaled corticosteroid preventer, four (45%) of whom reported poor adherence (usage < five days/week).
      Spirometry-- obtained out of the ryegrass pollen season-- demonstrated airflow obstruction in only seventeen patients (20%), and a bronchodilator response in only nine (11%).
      Eighty-four (99%) of 85 patients had allergic rhinitis symptoms spanning the ryegrass pollen season. Eighty-one (95%) of 85 patients had skin testing, serum specific IgE, or both performed. Of these, 100% were sensitized to ryegrass pollen. For ryegrass pollen, the mean skin prick diameter was 11 ± 6 mm and the serum specific IgE was 55 ± 34 kU/L (range 1-100kU/L). Total serum IgE was 459 ± 546kU/L (range 24-2229kU/L).
      Eighty (94%) of 85 patients reported outdoor exposure between 1700 and 2000 h on 21st November 2016. Airborne pollen levels were ‘extreme’ (102grains/m3) on the day.

      4. Discussion

      Ryegrass pollen sensitization, clinical allergic rhinitis, and acute allergen exposure are a risk factor trifecta for Melbourne thunderstorm asthma [

      AIHW. Allergic rhinitis ('hay fever') in Australia Canberra AIHW. 2011 [Viewed 26 May 2017]. Cat. no. ACM 23. :[Available from: http://www.aihw.gov.au/publication-detail/?id=10737420595.

      ,
      • Abramson M.
      • Kutin J.J.
      • Bailey M.
      • Raven J.
      • Dunster K.
      • Rolland J.
      • et al.
      Nasal allergies hayfever among young adults in Melbourne, Australia.
      ]. Our results have important implications for thunderstorm asthma prevention, not only in Melbourne but also for other regions across the globe where temperate ryegrass (Lolium perenne) is cultivated.
      Firstly, we confirm that allergic rhinitis and ryegrass pollen sensitization clearly define the adult population at risk for thunderstorm asthma. In Melbourne, allergic rhinitis affects up to 17% of the population, and should now be considered a condition with potentially serious consequences [

      AIHW. Allergic rhinitis ('hay fever') in Australia Canberra AIHW. 2011 [Viewed 26 May 2017]. Cat. no. ACM 23. :[Available from: http://www.aihw.gov.au/publication-detail/?id=10737420595.

      ,
      • Abramson M.
      • Kutin J.J.
      • Bailey M.
      • Raven J.
      • Dunster K.
      • Rolland J.
      • et al.
      Nasal allergies hayfever among young adults in Melbourne, Australia.
      ]. Ryegrass pollen sensitization should be confirmed and appropriate treatment offered, which may include nasal corticosteroids and specific allergen immunotherapy [
      • Hew M.
      • Sutherland M.
      • Thien F.
      • O'Hehir R.
      The Melbourne thunderstorm asthma event: can we avert another strike?.
      ].
      Secondly, exposure to the outdoors is the critical trigger for thunderstorm asthma. It is hypothesised ryegrass pollen grains (>35 μm in diameter) are ruptured by storm moisture into respirable 3 μm granules [
      • Bellomo R.
      • Gigliotti P.
      • Treloar A.
      • Holmes P.
      • Suphioglu C.
      • Singh M.B.
      Two consecutive thunderstorm associated epidemics of asthma in Melbourne. The possible role of rye grass pollen.
      ,
      • Suphioglu C.
      • Singh M.B.
      • Taylor P.
      • Knox R.B.
      • Bellomo R.
      • Holmes P.
      Mechanism of grass-pollen-induced asthma.
      ]. Thunderstorm downdrafts draw these granules to ground level mimicking aerosol challenges [
      • Marks G.B.
      Thunderstorm outflows preceding epidemics of asthma during spring and summer.
      ,
      • D'amato G.
      • Maesano I.
      • Molino A.
      • Vitale C.
      • D'Amato M.
      Thunderstorm-related asthma attacks.
      ]. Early warning systems should be developed to alert allergic rhinitis patients to stay indoors with windows shut before the onset potential thunderstorm epidemics.
      Our patients had a higher rate of allergic rhinitis (99%) than reported previously [
      • Bellomo R.
      • Gigliotti P.
      • Treloar A.
      • Holmes P.
      • Suphioglu C.
      • Singh M.B.
      Two consecutive thunderstorm associated epidemics of asthma in Melbourne. The possible role of rye grass pollen.
      ]. We are also the first to show universal (100%) ryegrass pollen sensitization among those tested with a combination of skin testing and serum specific IgE. In Melbourne, Bermuda sensitization often accompanies ryegrass sensitization, explaining its high prevalence. Fungal sensitization was not relevant for this event.
      Our outdoor exposure rate (94%) exceeds that of a previous questionnaire-based case-control study (38%) [
      • Girgis S.T.
      • Marks G.B.
      • Downs S.H.
      • Kolbe A.
      • Car G.N.
      • Paton R.
      Thunderstorm-associated asthma in an inland town in south-eastern Australia. Who is at risk?.
      ], and may be explained by the more detailed history available during clinical consultation.
      A prior diagnosis of asthma, or detectable airflow obstruction outside of the pollen season, was found in the minority. Although important, they are insensitive markers of risk. Asthma was underdiagnosed and undertreated in our cohort, exposing gaps in community asthma management [
      • Tay T.R.
      • Abramson M.J.
      • Hew M.
      Closing the million patient gap of uncontrolled asthma.
      ].
      By Australian rates, active smoking was under-represented in our cohort, and is probably not an important contributor to thunderstorm asthma.
      Our study has the usual constraints of an uncontrolled cohort, and is subject to recall bias for outdoors exposure history. Not all patients attended clinic, and four patients did not undergo allergen testing.
      Sensitization, clinical allergic rhinitis, and outdoor exposure to ryegrass pollen are critical contributors to thunderstorm asthma risk, and each requires preventive public health measures. Further investigation should focus on identifying more specific markers of susceptibility within this at-risk group.

      Acknowledgements

      The authors thank the team of Monash medical students who assisted with contacting patients; the Alfred hospital Clinical Performance Unit, Professor Frank Thien (Eastern health, Melbourne), the lung function lab (Alfred hospital) and the asthma nurses (Alfred hospital).

      Author statement

      JL, ROH and MH conceived and designed the study. JL, CK, MH collected data. JL and MH interpreted the data and were responsible for the first draft to which all authors contributed. All authors approved the final version.

      Competing interests

      Mark Hew has undertaken contracted research for AstraZeneca, Sanofi, Novartis, & GlaxoSmithKline; delivered Educational talks for GlaxoSmithKline, AstraZeneca & Novartis; Participated on advisory boards/consultancies for AstraZeneca, GSK & Seqirus; for all of which his employer (Alfred Health) has been reimbursed.

      Funding information

      Nil to declare.

      Ethics approval

      Alfred Health Research and Ethics department.

      Notation of prior abstract publication/presentation

      Thoracic Society of Australia and New Zealand Annual Scientific Meeting, 24–28th March 2017, Canberra, Australia.

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