Thunderstorm-asthma and pollen allergy

Melbourne Thunderstorm Asthma Deaths

21 November 2016: Melbourne, Australia

Thunderstorm Asthma incidents: Wikipedia1)https://en.wikipedia.org/wiki/Thunderstorm_asthma

  • 6 July 1983–7 July 1983: Birmingham, England
  • November 1987: Melbourne, Australia
  • 29 November 1989–30 November 1989: Melbourne, Australia
  • 24 July 1994–25 July 1994: London, England
  • 30 October 1997: Wagga Wagga, Australia
  • 4 June 2004: Naples, Italy
  • 2010: Melbourne, Australia
  • 2 November 2013: Ahvaz, Iran
  • 21 November 2016: Melbourne, Australia

 | Full Article Here

Abstract

Thunderstorms have been linked to asthma epidemics, especially during the pollen seasons, and there are descriptions of asthma outbreaks associated with thunderstorms, which occurred in several cities, prevalently in Europe (Birmingham and London in the UK and Napoli in Italy) and Australia (Melbourne and Wagga Wagga). Pollen grains can be carried by thunderstorm at ground level, where pollen rupture would be increased with release of allergenic biological aerosols of paucimicronic size, derived from the cytoplasm and which can penetrate deep into lower airways. In other words, there is evidence that under wet conditions or during thunderstorms, pollen grains may, after rupture by osmotic shock, release into the atmosphere part of their content, including respirable, allergen-carrying cytoplasmic starch granules (0.5–2.5 μm) or other paucimicronic components that can reach lower airways inducing asthma reactions in pollinosis patients. The thunderstorm-asthma outbreaks are characterized, at the beginning of thunderstorms by a rapid increase of visits for asthma in general practitioner or hospital emergency departments. Subjects without asthma symptoms, but affected by seasonal rhinitis can experience an asthma attack. No unusual levels of air pollution were noted at the time of the epidemics, but there was a strong association with high atmospheric concentrations of pollen grains such as grasses or other allergenic plant species. However, subjects affected by pollen allergy should be informed about a possible risk of asthma attack at the beginning of a thunderstorm during pollen season.


Medical Paper: Thunderstorm-asthma and pollen allergy

First published:  2006 December 6th  Authors: G. D'Amato, G. Liccardi, G. Frenguelli Title: Thunderstorm-asthma and pollen allergy Source: onlinelibrary.wiley.com | • Prof. Gennaro D'Amato Division of Pneumology and Allergology Department of Respiratory Diseases High Speciality Hospital ‘‘A. Cardarelli’’ Via Rione Sirignano, 10 80121 Napoli, Italy

There is evidence that thunderstorms can be associated with allergic asthma epidemics in pollinosis patients2)[Notes 1 – 16]

fn1 Suphioglu C, Singh MB, Taylor P, Knox RB. Mechanism of grass-pollen-induced asthma. Lancet 1992;339:569–572.

fn2 Knox RB. Grass pollen, thunderstorms and asthma. Clin Exp Allergy1993;23:354–356.

fn3 Packe GE, Ayres JG. Asthma outbreak during a thunderstorm. Lancet1985;ii:199–204.

fn4 Bellomo R, Gigliotti P, Treloar A, Holmes P, Suphioglu C, Singh MB. Two consecutive thunderstorm associated epidemic of asthma in Melbourne. Med J Aust1992;156:834–837.

fn5 Murray V, Venables K, Laing-Morton T, Partridge M, Williams D. Epidemic of asthma possibly related to thunderstorms. BMJ1994;309:131–132.

fn6 Wallis DN, Davidson AC, Weilch J et al. Clinical and immunological characteristics of patients with thunderstorm asthma. Eur Respir J 1995; 8:500s(Abstract).

fn7 Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ 1996; 312:601–604.

fn8 Celenza A, Fothergill J, Kupek E, Shaw RJ. Thunderstorms associated asthma: a detailed analysis of environmental factors. BMJ 1996; 312:604–607.

fn9 Bauman A. Asthma associated with thunderstorm. BMJ 1996; 312:590–591.

fn10 Venables KM, Allitt U, Collier CG, Emberlin J, Greig JB, Hardaker PJet al. Thunderstorm-related asthma – epidemic 24/25 June 1994. Clin Exp Allergy 1997; 27:725–736.

fn11 Newson R, Strachan D, Archibald E, Emberlin J, Hardaker P, Collier C. Effect of thunderstorms and airborne grass pollen on the incidence of acute asthma in England, 1990–1994. Thorax 1997; 52:669–670.

fn12 Antò JM, Sunyer J. Thunderstorms: a risk factor for asthma attacks. Thorax 1997; 52:669–670.

fn13 Newson R, Strachan D, Archibald E et al. Acute asthma epidemics, weather and pollen in England, 1987–1994. Eur Respir J 1998;11:694–701.

fn14 Girgis ST, Marks GB, Downs SH, Kolbe A, Car GN, Paton R. Thunderstorm-associated asthma in an inland town in southeastern Australia. Who is at risk? Eur Respir J 2000; 16:3–8.

fn15 Marks GB, Colquhoun JR, Girgis ST, Koski MH, Treloar ABA, Hansen Pet al. Thunderstorm outflows preceding epidemics of asthma during spring and summer. Thorax 2001; 56:468–471.

fn16 D’Amato G, Liccardi G, Viegi G, Baldacci S. Thunderstorm-associated asthma in pollinosis patients. BMJ 2005. Available at http://bmj.bmjjournals.com/cgi/eletters/309/6947/131/c.
during pollen seasons, and there is argument in favour of the possibility that thunderstorms concentrate at ground level pollen grains that release in atmosphere allergenic particles of respirable size after their rupture by osmotic shock3)[Notes 1 – 2]

fn1 Suphioglu C, Singh MB, Taylor P, Knox RB. Mechanism of grass-pollen-induced asthma. Lancet 1992; 339:569–572.

fn2 Knox RB. Grass pollen, thunderstorms and asthma. Clin Exp Allergy 1993; 23:354–356.

It has been demonstrated that changes in the weather, such as rain or humidity, may induce hydration of pollen grains and sometimes also their fragmentation, which generates atmospheric biological aerosols carrying allergens.4)[Notes 8,11,15]

fn8 Celenza A, Fothergill J, Kupek E, Shaw RJ. Thunderstorms associated asthma: a detailed analysis of environmental factors. BMJ 1996; 312:604–607.

fn11 Newson R, Strachan D, Archibald E, Emberlin J, Hardaker P, Collier C. Effect of thunderstorms and airborne grass pollen on the incidence of acute asthma in England, 1990–1994. Thorax 1997; 52:669–670.

fn15 Marks GB, Colquhoun JR, Girgis ST, Koski MH, Treloar ABA, Hansen Pet al. Thunderstorm outflows preceding epidemics of asthma during spring and summer. Thorax 2001; 56:468–471.

During the first phase of a thunderstorm, pollinosis subjects may inhale a high concentration of allergenic material dispersed in atmosphere, which can induce asthmatic reactions and sometimes even severe ones.5)[Notes 2,6,12,13]

fn2 Knox RB. Grass pollen, thunderstorms and asthma. Clin Exp Allergy 1993; 23:354–356

fn6 Wallis DN, Davidson AC, Weilch J et al. Clinical and immunological characteristics of patients with thunderstorm asthma. Eur Respir J 1995; 8:500s(Abstract).

fn12 Antò JM, Sunyer J. Thunderstorms: a risk factor for asthma attacks. Thorax 1997; 52:669–670.

fn13 Newson R, Strachan D, Archibald E et al. Acute asthma epidemics, weather and pollen in England, 1987–1994. Eur Respir J 1998; 11:694–701.

Fortunately, although it can induce severe asthma, outbreaks associated with thunderstorms are neither frequent nor responsible for high entity of disease exacerbations.6)[Notes 12,14,15]

fn12 Antò JM, Sunyer J. Thunderstorms: a risk factor for asthma attacks. Thorax 1997; 52:669–670.

fn14 Girgis ST, Marks GB, Downs SH, Kolbe A, Car GN, Paton R. Thunderstorm-associated asthma in an inland town in southeastern Australia. Who is at risk? Eur Respir J 2000; 16:3–8.

fn15 Marks GB, Colquhoun JR, Girgis ST, Koski MH, Treloar ABA, Hansen Pet al. Thunderstorm outflows preceding epidemics of asthma during spring and summer. Thorax 2001; 56:468–471.
However, the mechanisms involved in the release of allergens from pollens during thunderstorm should be known so that pollinosis patients can receive information about the risk of an asthma attack also in subjects affected only by seasonal allergic rhinitis.

Although thunderstorm-associated asthma outbreaks are not frequent, it is possible to observe in clinical practice single cases of patients with deterioration of the allergic respiratory symptoms during a thunderstorm7)[Notes 17a,18a]

fn17a Wardman AE, Stefani D, MacDonald JC. Thunderstorm-associated asthma or shortness of breath epidemic: a Canadian case report. Can Respir J 2002; 9:267–270.

fn18a Rosas I, McCartney HA, Payne RW, Calderon C, Lacey J, Chapela R et al.Analysis of the relationship between environmental factors (aeroallergens, air pollution and weather) and asthma emergency admissions to a hospital in Mexico City. Allergy 1998; 53:394–401.
and this possibility should be considered, because the frequency of thunderstorms is recently increased in some geographical areas, particularly in temperate and subtropical climate.

Allergenic pollen in the atmosphere

Although representing only a small proportion of the airborne particles present in the atmosphere, pollen grains can be causative agents of allergic respiratory responses in pollen allergic subjects, and pollinosis is now a public health problem.8)[Notes 19]

fn19 D’Amato G, Spieksma FT, Liccardi G, Jager S, Russo M, Kontou-Fili K et al.Pollen-related allergy in Europe. Position paper of the European Academy of Allergology and Clinical Immunology. Allergy 1998; 53:567–578.

Following Thommen’s postulates9)[Notes 20]

fn20 Thommen AA. Etiology of hay fever. N Y State J Med1930;437–441.
, to be allergenic, the pollen grains

• must contain antigens able to elicit a specific IgE-mediated response in atopic subjects;

• must be produced in high quantities;

• must be buoyant to be carried long distances;

• should be produced by plants that grow in abundance.

Thommen AA

Therefore, plants of major importance in pollen allergy are mainly those that rely on the wind as the carrier of the pollen and are defined anemophilous with allergens released by airborne pollens. In practice, only a few species, such as grass, pellitory, ragweed, mugwort, birch, olive, cypress, come into consideration as playing a major role in causing pollinosis, because they release in atmosphere large quantities of pollen during their flowering period.

In the European Community countries between 8% and 35% of young adults show IgE serum antibodies to grass pollen allergens10)[Notes 21]

fn21 Burney PGJ, Malmberg E, Chinn S, Jarvis D, Luczynska C, Lai E. The distribution of total and specific serum IgE in the European community respiratory health survey. J Allergy Clin Immunol 1997; 99:314–322.
and the cost of pollen allergy in terms of impaired work fitness, sick leave, consulting physicians and drugs, is very high.

During natural pollination, mature pollen grains are dehydrated when they are released by anthers at the dispersal time. Once the pollen grains come into contact with wet surface, they absorb water undergoing rapid metabolic changes jointly with ultrastructural modifications (Fig. 1). The pollinic allergens could be located in the pollen walls and/or in the cytoplasm and are rapidly released when the pollen grains come into contact with the oral, nasal or conjunctival mucosa, thereby inducing the appearance of pollinosis symptoms in sensitized patients. 11)[Notes 22,23]

fn22 Taylor PE, Flagan RC, Miguel AG, Valenta R, Glovsky MM. Birch pollen rupture and the release of aerosols of respirable allergens. Clin Exp Allergy 2004; 34:1591–1596.

fn23 Taylor PE, Hagan R, Valenta R, Glovsky MM. Release of allergens in respirable aerosols: a link between grass pollen and asthma. J Allergy Clin Immunol 2002; 109:51–56.
Sometimes, the cytoplasmic allergens are in the membrane surrounding starch granules and are released into the atmosphere when the pollen bursts under osmotic shock and can create a respirable allergenic aerosol.

figure-1-parietaria-pollen
Parietaria pollen bursting under osmotic shock with release of cytoplasmic fragments carrying allergens.

Figure 1.

In particular, it has been observed12)[Notes 22]

fn22 Taylor PE, Flagan RC, Miguel AG, Valenta R, Glovsky MM. Birch pollen rupture and the release of aerosols of respirable allergens. Clin Exp Allergy 2004; 34:1591–1596.
that fresh birch pollen can rupture in high humidity conditions, releasing an aerosol characterized by fragments of pollen cytoplasm ranging in size from 30 μnm to 4 μm and containing Bet v 1 allergen. Taylor et al.13)[Notes 23a]

fn23a Taylor PE, Hagan R, Valenta R, Glovsky MM. Release of allergens in respirable aerosols: a link between grass pollen and asthma. J Allergy Clin Immunol 2002; 109:51–56.
observed that about 65% of pollen grains grew a pollen tube up to 300-μm long prior to rupture and released their cytopasmic content in the high humidity context. The particles released, such as fragmented pollen cytoplasm, form an ultrafine aerosol. The same authors observed that grass anthers should be a site of pollen rupture and a source of fine particulate aerosols that contain pollen allergens.14)[Notes 23]

fn23 Taylor PE, Hagan R, Valenta R, Glovsky MM. Release of allergens in respirable aerosols: a link between grass pollen and asthma. J Allergy Clin Immunol 2002;109:51–56.

The concentration of allergenic pollen influences the degree of symptoms, but the relationship between allergen exposure, inflammation of airways and clinical symptoms is complex, and factors other than allergens are involved.15)[Notes 24]

fn24 Traidl-Hoffmann C, Kasche A, Menzel A, Jakob T, Thiel M, Ring J et al. Impact of pollen on human health: more than allergen carriers? Int Arch Allergy Immunol 2003; 131:1–13.
In particular, air pollution may contribute to the asthmatic activity as gaseous air pollution affects airways by inducing inflammation16)[Notes 25 – 28]

fn25 Schappi G, Taylor PE, Staff IA, Rolland JM, Suphioglu C. Immunologic significance of respirable atmospheric granules containing major birch allergen bet v 1. Allergy 1999; 54:478–83.

fn26 D’Amato G. Environmental urban factors (air pollution and allergens) and the rising trends in allergic respiratory diseases. Allergy 2002; 57 (Suppl.):30–33.

fn27 D’Amato G, Liccardi G, D’Amato M, Holgate ST. Environmental risk factors and allergic bronchial asthma. Clin Exp Allergy 2005; 35:1113–1124.

fn28 Antò JM, Sunyer J. Epidemic asthma and air pollution. In: D’AmatoG, HolgateST, editors. The impact of air pollution on respiratory health. Monograph of European Respiratory Society. Sheffield: ERS Journals, 2002:108–116.
and subjects living in urban areas tend to be more affected by plant-derived respiratory disorders than those living in rural areas,17)[Notes 29,39]

fn29 Riedler J, Eder W, Oberfeld G, Schrener M. Austrian children living on a farm have less hay fever, asthma and allergic sensitization. Clin Exp Allergy 2000;30:194–200.

fn30 Braun-Fahrlander C, Gassner M, Grize L, Neu U, Sennhauser FH, Varonier HS et al. Prevalence of hay fever and allergic sensitization in farmers’ children and their peers living in the same rurale community. SCARPOL team. Swiss study on childhood allergy and respiratory symptoms with respect to air pollution. Clin Exp Allergy 1999; 29:28–34.
and pollen allergens release is modified by exposure of pollen to environmental pollution.18)[Notes 25 – 27]

fn25 Schappi G, Taylor PE, Staff IA, Rolland JM, Suphioglu C. Immunologic significance of respirable atmospheric granules containing major birch allergen bet v 1. Allergy 1999; 54:478–83.

fn26 D’Amato G. Environmental urban factors (air pollution and allergens) and the rising trends in allergic respiratory diseases. Allergy 2002; 57(Suppl.):30–33.

fn27 D’Amato G, Liccardi G, D’Amato M, Holgate ST. Environmental risk factors and allergic bronchial asthma. Clin Exp Allergy 2005; 35:1113–1124.

Pollen grains penetrate into the upper respiratory tract but, because of their size, which is always greater than 10 μm of diameter, rarely reach the bronchial regions. However, bronchial asthma and its equivalents, such as irritative cough, are not infrequent in people affected by pollen-induced allergy.

Several hypotheses have been proposed to account for pollinosis-related symptoms in the lower respiratory tract at the bronchial level:19)[Notes 19,27]

fn19 D’Amato G, Spieksma FT, Liccardi G, Jager S, Russo M, Kontou-Fili K et al.Pollen-related allergy in Europe. Position paper of the European Academy of Allergology and Clinical Immunology. Allergy 1998; 53:567–578.

fn27 D’Amato G, Liccardi G, D’Amato M, Holgate ST. Environmental risk factors and allergic bronchial asthma. Clin Exp Allergy 2005; 35:1113–1124.

• Absorption of allergen in the nose and subsequent transportation to the lower airways.

• Reflex mechanisms inducing bronchial involvement after a nasal reaction.

• Inhalation and penetration of small particles carrying pollen allergen into the lower respiratory region.

hypotheses to account for pollinosis-related symptoms

The discovery of airborne-allergen-carrying particles much smaller than pollen grains, such as those released by pollens during weather perturbations, particularly thunderstorm and rainfall, provided a possible explanation. In other words, the existence of allergen-carrying airborne particles much smaller than pollen grains (paucimicronic particles) can explain bronchial symptoms affecting subjects during the pollen season or a thunderstorm20)[Notes 1,6-10]

fn1 Suphioglu C, Singh MB, Taylor P, Knox RB. Mechanism of grass-pollen-induced asthma. Lancet 1992; 339:569–572.

fn6 Wallis DN, Davidson AC, Weilch J et al. Clinical and immunological characteristics of patients with thunderstorm asthma. Eur Respir J 1995; 8:500s(Abstract).

fn7 Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ 1996; 312:601–604.

fn8 Celenza A, Fothergill J, Kupek E, Shaw RJ. Thunderstorms associated asthma: a detailed analysis of environmental factors. BMJ 1996; 312:604–607.

fn9 Bauman A. Asthma associated with thunderstorm. BMJ 1996; 312:590–591.

fn10 Venables KM, Allitt U, Collier CG, Emberlin J, Greig JB, Hardaker PJet al. Thunderstorm-related asthma – epidemic 24/25 June 1994. Clin Exp Allergy 1997; 27:725–736.
(Table 1).

Table 1.  Airborne small (paucimicronic) allergen-carrying particles

Starch granules and other components of the cytoplasm of pollen grains, released into the atmosphere under wet conditions, and responsible for thunderstorm-associated bronchial asthma.

Nonpollen plant parts from inflorescences, leaves or Ubisch bodies (spheroidal structures that develop in the anthers of many higher plants and that contain allergens).

Nonplant particulate matter (allergens transferred through physical contact or by leaching from the surface of the pollen grain to other airborne small particles).

Pollen fragments (are not frequently found and can derive from rupture of pollen grains during thunderstorms).

Thanks to their size; these paucimicronic particles can penetrate deep into the airways inducing asthma in sensitized atopic subjects.

In the context of paucimicronic particles, there are orbicules, small granules (1–5 μm) or droplets developed from anther tissues, loaded with allergens and there is suggestion that they play a role in allergic asthma contributing to form a respirable aerosol during the pollen season.21)[Notes 27,31-33]

fn27 D’Amato G, Liccardi G, D’Amato M, Holgate ST. Environmental risk factors and allergic bronchial asthma. Clin Exp Allergy2005;35:1113–1124.

fn31 El-Ghazaly G, Takahashi Y, Nilsson S, Grafstroem E, Berggren B. Orbicules in Betula pendula and their possible role in allergy. Grana 1995; 34:300–304.

fn32 Vinckier S, Smets E. The potential role of orbicules as vector of allergens. Allergy 2001; 56:1129–1136.

fn33 D’Amato G. Airborne paucimicronic allergen-carrying particles and seasonal respiratory allergy. Allergy 2001; 56:1109–1111.

Thunderstorms and allergic asthma epidemics in pollinosis subjects during pollen season

Rainfall is usually known to remove pollen from the air but that is not always correct, because studies have revealed that allergens leave the pollen surface almost instantly, usually within seconds, on contact with water.

Thunderstorm-asthma outbreaks have been described in various cities such as Birmingham (UK),22)[Notes 3]

fn3 Packe GE, Ayres JG. Asthma outbreak during a thunderstorm. Lancet 1985; ii:199–204.
London (UK),23)[Notes 7a,10a]

fn7a Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ 1996; 312:601–604.

fn10a Venables KM, Allitt U, Collier CG, Emberlin J, Greig JB, Hardaker PJet al. Thunderstorm-related asthma – epidemic 24/25 June 1994. Clin Exp Allergy 1997; 27:725–736.
Melbourne (Australia),24)[Notes 4a]

fn4a Bellomo R, Gigliotti P, Treloar A, Holmes P, Suphioglu C, Singh MB. Two consecutive thunderstorm associated epidemic of asthma in Melbourne. Med J Aust 1992; 156:834–837.
Wagga Wagga (Australia)25)[Notes 14a]

fn14a Girgis ST, Marks GB, Downs SH, Kolbe A, Car GN, Paton R. Thunderstorm-associated asthma in an inland town in southeastern Australia. Who is at risk? Eur Respir J 2000; 16:3–8.
and Naples (Italy),26)[Notes 16a]

fn16a D’Amato G, Liccardi G, Viegi G, Baldacci S. Thunderstorm-associated asthma in pollinosis patients. BMJ 2005. Available at http://bmj.bmjjournals.com/cgi/eletters/309/6947/131/c.
but there are case reports in other cities.27)[Notes 17b,18b]

fn17b Wardman AE, Stefani D, MacDonald JC. Thunderstorm-associated asthma or shortness of breath epidemic: a Canadian case report. Can Respir J 2002; 9:267–270.

fn18b Rosas I, McCartney HA, Payne RW, Calderon C, Lacey J, Chapela R et al.Analysis of the relationship between environmental factors (aeroallergens, air pollution and weather) and asthma emergency admissions to a hospital in Mexico City. Allergy 1998; 53:394–401.

One of the first observations regarding thunderstorms and asthma outbreaks was provided by Packe and Ayres28)Packe GE, Ayres JG. Asthma outbreak during a thunderstorm. Lancet1985;ii:199–204. at the East Birmingham Hospital, Birmingham, UK, on 6 and 7 July 1983. These authors describe a striking increase in the number of asthma emergency room visit admissions during the hours of a thunderstorm. In a period of 36 h, 26 asthma cases were treated in the emergency room, compared with a daily average of two or three cases in the days preceding the outbreak.

Another asthma outbreak occurred in London coinciding with a heavy thunderstorm on the 24 June 1994, when a large increase was observed in the number of visits for asthma at the emergency departments of London and the southwest of England, and several patients examined, who were not known to be asthmatics or were affected only by seasonal rhinitis, experienced an asthma attack29)[Notes 7b,10b]

fn7b Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ 1996; 312:601–604.

fn10b Venables KM, Allitt U, Collier CG, Emberlin J, Greig JB, Hardaker PJet al. Thunderstorm-related asthma – epidemic 24/25 June 1994. Clin Exp Allergy 1997; 27:725–736.

The epidemic had a sudden onset on 24 June 1994; 640 patients with asthma or other airways disease attended during 30 h from 18.00 on 24 June, nearly 10 times the expected number. Over half (365) the patients were aged 21–40. A history of hay fever was recorded in 403 patients; for 283 patients, this was the first known attack of asthma; a history of chronic obstructive airways disease was recorded in 12 patients. In all, 104 patients were admitted (including 5 to an intensive care unit). A total of 604 patients with wheezing and shortness of breath were seen in several departments, compared with an expected number of 66.6.30)[Notes 7]

fn7 Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ 1996; 312:601–604.

The results confirm asthma epidemic, with almost 10 times the usual number of patients presenting during 30 h and an excess of 574 patients attributable to the epidemic.31)[Notes 7b,10b]

fn7b Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ1996;312:601–604.

fn10b Venables KM, Allitt U, Collier CG, Emberlin J, Greig JB, Hardaker PJet al. Thunderstorm-related asthma – epidemic 24/25 June 1994. Clin Exp Allergy 1997;27:725–736.
The outbreak was not restricted to the London area, although the number of patients presenting to accident and emergency departments on the night of 24 June 1994 was greater in the Thames regions than in other regions in England. Moreover, not all affected patients attended hospital and this epidemic was the largest outbreak ever recorded.

Other asthma outbreaks during thunderstorms were described in Melbourne, Australia,32)[Notes 4b]

fn4b Bellomo R, Gigliotti P, Treloar A, Holmes P, Suphioglu C, Singh MB. Two consecutive thunderstorm associated epidemic of asthma in Melbourne. Med J Aust 1992; 156:834–837.
where two large asthma outbreaks coincided with thunderstorms. In addition, these events were followed by a rapid increase in hospital or general practitioner visits for asthma. Taking into account the Melbourne experience, a similar mechanism could have been involved, although other factors may have also contributed.

Other asthma outbreaks occurred in Wagga Wagga (southern Australia) on 30 October 199733)[Notes 14b]

fn14b Girgis ST, Marks GB, Downs SH, Kolbe A, Car GN, Paton R. Thunderstorm-associated asthma in an inland town in southeastern Australia. Who is at risk? Eur Respir J 2000; 16:3–8.
and in Naples, Italy on 4 June 2004.34)[Notes 16b]

fn16b D’Amato G, Liccardi G, Viegi G, Baldacci S. Thunderstorm-associated asthma in pollinosis patients. BMJ 2005. Available at http://bmj.bmjjournals.com/cgi/eletters/309/6947/131/c.

In Wagga Wagga, 215 asthmatic subjects attended the local emergency department, 41 of whom required admission to hospital. Marks et al. 35)[Notes 15]

fn15 Marks GB, Colquhoun JR, Girgis ST, Koski MH, Treloar ABA, Hansen Pet al. Thunderstorm outflows preceding epidemics of asthma during spring and summer. Thorax 2001; 56:468–471.
demonstrated that the arrival of a thunderstorm outflow was accompanied by a large increase in the concentration of ruptured pollen grains in ambient air and they observed that in a large region of south eastern Australia, the incidence of excess hospital attendances for asthma during late spring and summer was strongly linked to the occurrence of thunderstorm outflows.

It seems likely that the outflow of cold air associated with a thunderstorm rather than electrical activity, thunder or rain alone, is responsible for the observed event.

During the episode of thunderstorm-associated asthma registered in Naples on 4 June 2004 (between 1.30 and 2.00am), six adults (three women and three men between 38 and 60 years old) and a girl of 11 years old had attacks of severe bronchial asthma, which was nearly fatal in one case. All patients received treatment in emergency departments and one was admitted to an intensive care unit for very severe bronchial obstruction and acute respiratory insufficiency.

All subjects were outdoors when the thunderstorm struck. The most severe case, a 60-year-old woman sensitized only to Parietaria pollen allergens, soon began to show symptoms of intense dyspnoea, which gradually worsened. She was taken to hospital where she was intubated and given high intravenous doses of corticosteroids. She was discharged a few days later. She had previously suffered from seasonal asthma, but had been asthma-free for the past few years and did not need continuous therapy. None of the other six subjects regularly took antiallergic and/or antiasthma drugs. Four had a history of asthma, whereas two had a history of only rhinitis.

We found that all seven patients were sensitized with allergic respiratory symptoms upon exposure to Parietaria pollen but were not sensitized to grasses.36)[Notes 16c]

fn16c D’Amato G, Liccardi G, Viegi G, Baldacci S. Thunderstorm-associated asthma in pollinosis patients. BMJ 2005. Available at http://bmj.bmjjournals.com/cgi/eletters/309/6947/131/c.

Parietaria is an urticacea that is widespread in the Naples area with a spring and summer pollen season in part contemporaneous with that of grasses.37)[Notes 34]

fn34 D’Amato G, Ruffilli A, Ortolani C. Allergenic significance of Parietaria(pellitory-of-the-wall) pollen. In: D’AmatoG, SpieksmaF, BoniniS, editors. Allergenic pollen and pollinosis in Europe. Oxford: Blackwell Scientific Publications, 1991:113–118.
During the thunderstorm, the concentration of airborne Parietaria pollen grains was particularly high with a peak of 144 grains/m3 being recorded on June 3. Air pollution levels for both gaseous and particulate components based on the hourly concentrations of nitric dioxide, ozone and respirable particulate matter were not particularly high in Naples on June 3 and 4.

Subjects with sensitization to Parietaria, who were indoors in Naples with the windows closed during the night between 3 and 4 June, did not experience asthma attacks. There was evidence that thunderstorm-induced asthma was related to the Parietaria pollen allergens.

Possible mechanisms for thunderstorm asthma

What is most frequently hypothesized is that dry updrafts entrain whole pollens into the high humidity at the cloud base of a thunderstorm where pollens may rupture and cold downdrafts carry pollen fragments to ground level. In other words, at the onset of a thunderstorm, pollen fragments are carried to ground level where outflows distribute them. As a consequence, there is high respirable allergen load in the air.

Taylor et al.38)[Notes 23b]

fn23b Taylor PE, Hagan R, Valenta R, Glovsky MM. Release of allergens in respirable aerosols: a link between grass pollen and asthma. J Allergy Clin Immunol 2002; 109:51–56.
hypothesized that the turbulent front of the advancing outflow releases more pollen from flowering grasses, and then may entrain them into the cloud base. Strong electric fields develop in the thunderstorm. Positive ions are released from the ground and attach to particles and electric charge may enhance pollen rupture.

Grass pollens after rupture by osmotic shock during thunderstorms release large amounts of paucimicronic allergenic particles, i.e. cytoplasmatic starch granules containing grass allergens. Other pollens, such as those of Parietaria, which have no starch granule in the cytoplasm can release other paucimicronic cytoplasmic components carrying allergens. Because of their very small size, these microparticles can penetrate the lower airways inducing the appearance of bronchial allergic symptoms.

Suphioglu et al.39)[Notes 1]

fn1 Suphioglu C, Singh MB, Taylor P, Knox RB. Mechanism of grass-pollen-induced asthma. Lancet 1992;339:569–572.
showed that rye grass pollen grains contain a large quantity of starch granules coated with the allergens. While levels of chemical air pollution on epidemic days were below or similar to levels in a control period. This observation led to the hypothesis that pollen grains are ruptured in rainwater by osmotic shock, with each grain releasing around 700 starch granules small enough to penetrate the airways and trigger asthma attacks in previously sensitized subjects. Although much remains to be discovered about the relationship between an increase in the number of asthma attacks and thunderstorms, reasonable evidence exists in favour of a casual link between them.40)Antò J. Epidemic asthma. In: HolgateST, BousheyHA, FabbriLM, editors. Difficult asthma. UK: Martin Dunitz, 1999:333–340. If this is the case, asthmatics sensitized to pollen allergens may be at risk of suffering asthma attacks during thunderstorms. Depending on the size of the population at risk, thunderstorm-associated asthma outbreaks may threaten the operative capacity of health services, as was the case in London. Therefore, it could be of interest to establish whether some risk factors may predict the occurrence of asthma outbreaks in such a way that early-warning systems can be developed. With this approach, and using the same data set alluded above, Newson et al. identified 56 asthma epidemics defined as periods of exceptionally high asthma admission counts compared with predictions of a log-linear autoregressive model.41)[Notes 11a]

fn11a Newson R, Strachan D, Archibald E, Emberlin J, Hardaker P, Collier C. Effect of thunderstorms and airborne grass pollen on the incidence of acute asthma in England, 1990–1994. Thorax 1997; 52:669–670.

However, although thunderstorms and high grass pollen levels preceded asthma epidemics, most thunderstorms, even those coincident with high grass pollen levels in atmosphere, were not followed by asthma epidemics. The authors concluded that using predictions of thunderstorms during periods of high pollen counts as an early-warning system of asthma epidemics would produce too many false alarms to be accepted42)[Notes 12]

fn12 Antò JM, Sunyer J. Thunderstorms: a risk factor for asthma attacks. Thorax 1997; 52:669–670.
A more systematic investigation of the relationship between an abrupt increase in the number of asthma attacks and the occurrence of thunderstorms has been provided by Newson et al..43)[Notes 11b]

fn11b Newson R, Strachan D, Archibald E, Emberlin J, Hardaker P, Collier C. Effect of thunderstorms and airborne grass pollen on the incidence of acute asthma in England, 1990–1994. Thorax 1997; 52:669–670.
Daily numbers of sferic densities, a marker of lightning flashes during thunderstorms, were obtained for each area, and their connection with the number of asthma admissions was evaluated by means of log-linear autoregressive models. Although typical thunderstorms days were not associated with large asthma epidemics, the presence of very large sferic densities was associated with a moderate enhancement in hospital admissions for asthma chrisis. High level of sferic densities were associated with a relative risk of approximately 25% in both the 0–14 years and 15 years and over age groups, whereas the excess risk associated with moderate sferic densities was smaller, but statistically significant.44)[Notes 35]

fn35 Antò J. Epidemic asthma. In: HolgateST, BousheyHA, FabbriLM, editors. Difficult asthma. UK: Martin Dunitz, 1999:333–340.
On the basis of the Melbourne hypothesis, the authors were able to obtain daily grass pollen counts in five regional health authorities and found that high pollen counts for the previous 5 days were associated with amplification of the excess risk associated with thunderstorms.

Unfortunately, the data of Newson et al.45)[Notes 11c]

fn11c Newson R, Strachan D, Archibald E, Emberlin J, Hardaker P, Collier C. Effect of thunderstorms and airborne grass pollen on the incidence of acute asthma in England, 1990–1994. Thorax 1997; 52:669–670.
do not support the possibility of predicting asthma outbreaks using meteorological data and pollen counts.

Finally, no moulds or viruses were involved in the epidemics.

Conclusions

There is evidence that thunderstorms trigger epidemics of exacerbations of asthma during the pollen season by washing down pollen grains and concentrating them in a band of air at ground level. Pollen grains may, after contact with rain or humidity, release part of their cytoplasmic content, including respirable, allergen-carrying paucimicronic particles.

Cytoplasmic granules of small size are released from the pollen grains by contact with rainwater. As a consequence, at the onset of a thunderstorm, there is a high respirable allergen load in the air and these conditions might expose susceptible subjects to a high increase of pollen allergens in the atmosphere.

Thunderstorm-associated asthma is a dramatic example of the allergenic potential of pollen antigens. Pollen-allergic patients who encounter the allergenic cloud would be more susceptible to undergo an asthma attack.

Subjects allergic to pollen, who are in the path of the thunderstorm outflow, are likely to inhale airborne pollen allergens and to experience an airway asthmatic response.

The characteristics of described epidemics of thunderstorm-associated asthma can be summarized as follows:

• There is a link between asthma epidemics and thunderstorm.

• The epidemics related to thunderstorm are limited to seasons when there are high atmospheric concentrations of airborne allergenic pollens.

• There is a close temporal association between the start of the thunderstorm and the onset of epidemics.

• There are not high levels of gaseous and particulate components of air pollution.

• Subjects with pollen allergy, who stay indoors with window closed during thunderstorm, are not involved.

• There is a major risk for the subjects who are not under antiasthma correct treatment, but subjects with allergic rhinitis and without previous asthma can experience severe bronchoconstriction.

characteristics of thunderstorm-associated asthma

In the light of the above, subjects affected by pollen allergy should be alert to the danger of being outdoors during a thunderstorm in the pollen season, as such events may be an important cause of severe exacerbations of asthma

In other words, when asthmatic patients realize that a thunderstorm is approaching the best thing for them to do is to stay indoors, with windows closed.

Related:

Thunderstorm-related asthma: what happens and why
Authors
G. D’Amato, C. Vitale, M. D’Amato, L. Cecchi, G. Liccardi, A. Molino, A. Vatrella, A. Sanduzzi, C. Maesano, I. Annesi-Maesano
Published Date
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References   [ + ]

1. https://en.wikipedia.org/wiki/Thunderstorm_asthma
2. [Notes 1 – 16]

fn1 Suphioglu C, Singh MB, Taylor P, Knox RB. Mechanism of grass-pollen-induced asthma. Lancet 1992;339:569–572.

fn2 Knox RB. Grass pollen, thunderstorms and asthma. Clin Exp Allergy1993;23:354–356.

fn3 Packe GE, Ayres JG. Asthma outbreak during a thunderstorm. Lancet1985;ii:199–204.

fn4 Bellomo R, Gigliotti P, Treloar A, Holmes P, Suphioglu C, Singh MB. Two consecutive thunderstorm associated epidemic of asthma in Melbourne. Med J Aust1992;156:834–837.

fn5 Murray V, Venables K, Laing-Morton T, Partridge M, Williams D. Epidemic of asthma possibly related to thunderstorms. BMJ1994;309:131–132.

fn6 Wallis DN, Davidson AC, Weilch J et al. Clinical and immunological characteristics of patients with thunderstorm asthma. Eur Respir J 1995; 8:500s(Abstract).

fn7 Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ 1996; 312:601–604.

fn8 Celenza A, Fothergill J, Kupek E, Shaw RJ. Thunderstorms associated asthma: a detailed analysis of environmental factors. BMJ 1996; 312:604–607.

fn9 Bauman A. Asthma associated with thunderstorm. BMJ 1996; 312:590–591.

fn10 Venables KM, Allitt U, Collier CG, Emberlin J, Greig JB, Hardaker PJet al. Thunderstorm-related asthma – epidemic 24/25 June 1994. Clin Exp Allergy 1997; 27:725–736.

fn11 Newson R, Strachan D, Archibald E, Emberlin J, Hardaker P, Collier C. Effect of thunderstorms and airborne grass pollen on the incidence of acute asthma in England, 1990–1994. Thorax 1997; 52:669–670.

fn12 Antò JM, Sunyer J. Thunderstorms: a risk factor for asthma attacks. Thorax 1997; 52:669–670.

fn13 Newson R, Strachan D, Archibald E et al. Acute asthma epidemics, weather and pollen in England, 1987–1994. Eur Respir J 1998;11:694–701.

fn14 Girgis ST, Marks GB, Downs SH, Kolbe A, Car GN, Paton R. Thunderstorm-associated asthma in an inland town in southeastern Australia. Who is at risk? Eur Respir J 2000; 16:3–8.

fn15 Marks GB, Colquhoun JR, Girgis ST, Koski MH, Treloar ABA, Hansen Pet al. Thunderstorm outflows preceding epidemics of asthma during spring and summer. Thorax 2001; 56:468–471.

fn16 D’Amato G, Liccardi G, Viegi G, Baldacci S. Thunderstorm-associated asthma in pollinosis patients. BMJ 2005. Available at http://bmj.bmjjournals.com/cgi/eletters/309/6947/131/c.
3. [Notes 1 – 2]

fn1 Suphioglu C, Singh MB, Taylor P, Knox RB. Mechanism of grass-pollen-induced asthma. Lancet 1992; 339:569–572.

fn2 Knox RB. Grass pollen, thunderstorms and asthma. Clin Exp Allergy 1993; 23:354–356.
4. [Notes 8,11,15]

fn8 Celenza A, Fothergill J, Kupek E, Shaw RJ. Thunderstorms associated asthma: a detailed analysis of environmental factors. BMJ 1996; 312:604–607.

fn11 Newson R, Strachan D, Archibald E, Emberlin J, Hardaker P, Collier C. Effect of thunderstorms and airborne grass pollen on the incidence of acute asthma in England, 1990–1994. Thorax 1997; 52:669–670.

fn15 Marks GB, Colquhoun JR, Girgis ST, Koski MH, Treloar ABA, Hansen Pet al. Thunderstorm outflows preceding epidemics of asthma during spring and summer. Thorax 2001; 56:468–471.
5. [Notes 2,6,12,13]

fn2 Knox RB. Grass pollen, thunderstorms and asthma. Clin Exp Allergy 1993; 23:354–356

fn6 Wallis DN, Davidson AC, Weilch J et al. Clinical and immunological characteristics of patients with thunderstorm asthma. Eur Respir J 1995; 8:500s(Abstract).

fn12 Antò JM, Sunyer J. Thunderstorms: a risk factor for asthma attacks. Thorax 1997; 52:669–670.

fn13 Newson R, Strachan D, Archibald E et al. Acute asthma epidemics, weather and pollen in England, 1987–1994. Eur Respir J 1998; 11:694–701.
6. [Notes 12,14,15]

fn12 Antò JM, Sunyer J. Thunderstorms: a risk factor for asthma attacks. Thorax 1997; 52:669–670.

fn14 Girgis ST, Marks GB, Downs SH, Kolbe A, Car GN, Paton R. Thunderstorm-associated asthma in an inland town in southeastern Australia. Who is at risk? Eur Respir J 2000; 16:3–8.

fn15 Marks GB, Colquhoun JR, Girgis ST, Koski MH, Treloar ABA, Hansen Pet al. Thunderstorm outflows preceding epidemics of asthma during spring and summer. Thorax 2001; 56:468–471.
7. [Notes 17a,18a]

fn17a Wardman AE, Stefani D, MacDonald JC. Thunderstorm-associated asthma or shortness of breath epidemic: a Canadian case report. Can Respir J 2002; 9:267–270.

fn18a Rosas I, McCartney HA, Payne RW, Calderon C, Lacey J, Chapela R et al.Analysis of the relationship between environmental factors (aeroallergens, air pollution and weather) and asthma emergency admissions to a hospital in Mexico City. Allergy 1998; 53:394–401.
8. [Notes 19]

fn19 D’Amato G, Spieksma FT, Liccardi G, Jager S, Russo M, Kontou-Fili K et al.Pollen-related allergy in Europe. Position paper of the European Academy of Allergology and Clinical Immunology. Allergy 1998; 53:567–578.
9. [Notes 20]

fn20 Thommen AA. Etiology of hay fever. N Y State J Med1930;437–441.
10. [Notes 21]

fn21 Burney PGJ, Malmberg E, Chinn S, Jarvis D, Luczynska C, Lai E. The distribution of total and specific serum IgE in the European community respiratory health survey. J Allergy Clin Immunol 1997; 99:314–322.
11. [Notes 22,23]

fn22 Taylor PE, Flagan RC, Miguel AG, Valenta R, Glovsky MM. Birch pollen rupture and the release of aerosols of respirable allergens. Clin Exp Allergy 2004; 34:1591–1596.

fn23 Taylor PE, Hagan R, Valenta R, Glovsky MM. Release of allergens in respirable aerosols: a link between grass pollen and asthma. J Allergy Clin Immunol 2002; 109:51–56.
12. [Notes 22]

fn22 Taylor PE, Flagan RC, Miguel AG, Valenta R, Glovsky MM. Birch pollen rupture and the release of aerosols of respirable allergens. Clin Exp Allergy 2004; 34:1591–1596.
13. [Notes 23a]

fn23a Taylor PE, Hagan R, Valenta R, Glovsky MM. Release of allergens in respirable aerosols: a link between grass pollen and asthma. J Allergy Clin Immunol 2002; 109:51–56.
14. [Notes 23]

fn23 Taylor PE, Hagan R, Valenta R, Glovsky MM. Release of allergens in respirable aerosols: a link between grass pollen and asthma. J Allergy Clin Immunol 2002;109:51–56.
15. [Notes 24]

fn24 Traidl-Hoffmann C, Kasche A, Menzel A, Jakob T, Thiel M, Ring J et al. Impact of pollen on human health: more than allergen carriers? Int Arch Allergy Immunol 2003; 131:1–13.
16. [Notes 25 – 28]

fn25 Schappi G, Taylor PE, Staff IA, Rolland JM, Suphioglu C. Immunologic significance of respirable atmospheric granules containing major birch allergen bet v 1. Allergy 1999; 54:478–83.

fn26 D’Amato G. Environmental urban factors (air pollution and allergens) and the rising trends in allergic respiratory diseases. Allergy 2002; 57 (Suppl.):30–33.

fn27 D’Amato G, Liccardi G, D’Amato M, Holgate ST. Environmental risk factors and allergic bronchial asthma. Clin Exp Allergy 2005; 35:1113–1124.

fn28 Antò JM, Sunyer J. Epidemic asthma and air pollution. In: D’AmatoG, HolgateST, editors. The impact of air pollution on respiratory health. Monograph of European Respiratory Society. Sheffield: ERS Journals, 2002:108–116.
17. [Notes 29,39]

fn29 Riedler J, Eder W, Oberfeld G, Schrener M. Austrian children living on a farm have less hay fever, asthma and allergic sensitization. Clin Exp Allergy 2000;30:194–200.

fn30 Braun-Fahrlander C, Gassner M, Grize L, Neu U, Sennhauser FH, Varonier HS et al. Prevalence of hay fever and allergic sensitization in farmers’ children and their peers living in the same rurale community. SCARPOL team. Swiss study on childhood allergy and respiratory symptoms with respect to air pollution. Clin Exp Allergy 1999; 29:28–34.
18. [Notes 25 – 27]

fn25 Schappi G, Taylor PE, Staff IA, Rolland JM, Suphioglu C. Immunologic significance of respirable atmospheric granules containing major birch allergen bet v 1. Allergy 1999; 54:478–83.

fn26 D’Amato G. Environmental urban factors (air pollution and allergens) and the rising trends in allergic respiratory diseases. Allergy 2002; 57(Suppl.):30–33.

fn27 D’Amato G, Liccardi G, D’Amato M, Holgate ST. Environmental risk factors and allergic bronchial asthma. Clin Exp Allergy 2005; 35:1113–1124.
19. [Notes 19,27]

fn19 D’Amato G, Spieksma FT, Liccardi G, Jager S, Russo M, Kontou-Fili K et al.Pollen-related allergy in Europe. Position paper of the European Academy of Allergology and Clinical Immunology. Allergy 1998; 53:567–578.

fn27 D’Amato G, Liccardi G, D’Amato M, Holgate ST. Environmental risk factors and allergic bronchial asthma. Clin Exp Allergy 2005; 35:1113–1124.
20. [Notes 1,6-10]

fn1 Suphioglu C, Singh MB, Taylor P, Knox RB. Mechanism of grass-pollen-induced asthma. Lancet 1992; 339:569–572.

fn6 Wallis DN, Davidson AC, Weilch J et al. Clinical and immunological characteristics of patients with thunderstorm asthma. Eur Respir J 1995; 8:500s(Abstract).

fn7 Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ 1996; 312:601–604.

fn8 Celenza A, Fothergill J, Kupek E, Shaw RJ. Thunderstorms associated asthma: a detailed analysis of environmental factors. BMJ 1996; 312:604–607.

fn9 Bauman A. Asthma associated with thunderstorm. BMJ 1996; 312:590–591.

fn10 Venables KM, Allitt U, Collier CG, Emberlin J, Greig JB, Hardaker PJet al. Thunderstorm-related asthma – epidemic 24/25 June 1994. Clin Exp Allergy 1997; 27:725–736.
21. [Notes 27,31-33]

fn27 D’Amato G, Liccardi G, D’Amato M, Holgate ST. Environmental risk factors and allergic bronchial asthma. Clin Exp Allergy2005;35:1113–1124.

fn31 El-Ghazaly G, Takahashi Y, Nilsson S, Grafstroem E, Berggren B. Orbicules in Betula pendula and their possible role in allergy. Grana 1995; 34:300–304.

fn32 Vinckier S, Smets E. The potential role of orbicules as vector of allergens. Allergy 2001; 56:1129–1136.

fn33 D’Amato G. Airborne paucimicronic allergen-carrying particles and seasonal respiratory allergy. Allergy 2001; 56:1109–1111.
22. [Notes 3]

fn3 Packe GE, Ayres JG. Asthma outbreak during a thunderstorm. Lancet 1985; ii:199–204.
23. [Notes 7a,10a]

fn7a Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ 1996; 312:601–604.

fn10a Venables KM, Allitt U, Collier CG, Emberlin J, Greig JB, Hardaker PJet al. Thunderstorm-related asthma – epidemic 24/25 June 1994. Clin Exp Allergy 1997; 27:725–736.
24. [Notes 4a]

fn4a Bellomo R, Gigliotti P, Treloar A, Holmes P, Suphioglu C, Singh MB. Two consecutive thunderstorm associated epidemic of asthma in Melbourne. Med J Aust 1992; 156:834–837.
25. [Notes 14a]

fn14a Girgis ST, Marks GB, Downs SH, Kolbe A, Car GN, Paton R. Thunderstorm-associated asthma in an inland town in southeastern Australia. Who is at risk? Eur Respir J 2000; 16:3–8.
26. [Notes 16a]

fn16a D’Amato G, Liccardi G, Viegi G, Baldacci S. Thunderstorm-associated asthma in pollinosis patients. BMJ 2005. Available at http://bmj.bmjjournals.com/cgi/eletters/309/6947/131/c.
27. [Notes 17b,18b]

fn17b Wardman AE, Stefani D, MacDonald JC. Thunderstorm-associated asthma or shortness of breath epidemic: a Canadian case report. Can Respir J 2002; 9:267–270.

fn18b Rosas I, McCartney HA, Payne RW, Calderon C, Lacey J, Chapela R et al.Analysis of the relationship between environmental factors (aeroallergens, air pollution and weather) and asthma emergency admissions to a hospital in Mexico City. Allergy 1998; 53:394–401.
28. Packe GE, Ayres JG. Asthma outbreak during a thunderstorm. Lancet1985;ii:199–204.
29. [Notes 7b,10b]

fn7b Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ 1996; 312:601–604.

fn10b Venables KM, Allitt U, Collier CG, Emberlin J, Greig JB, Hardaker PJet al. Thunderstorm-related asthma – epidemic 24/25 June 1994. Clin Exp Allergy 1997; 27:725–736.
30. [Notes 7]

fn7 Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ 1996; 312:601–604.
31. [Notes 7b,10b]

fn7b Thames Regions Accident and Emergency Trainer Association, Davidson AC, Emberlin J, Cook AD, Venables KM. A major outbreak of asthma associated with a thunderstorm. BMJ1996;312:601–604.

fn10b Venables KM, Allitt U, Collier CG, Emberlin J, Greig JB, Hardaker PJet al. Thunderstorm-related asthma – epidemic 24/25 June 1994. Clin Exp Allergy 1997;27:725–736.
32. [Notes 4b]

fn4b Bellomo R, Gigliotti P, Treloar A, Holmes P, Suphioglu C, Singh MB. Two consecutive thunderstorm associated epidemic of asthma in Melbourne. Med J Aust 1992; 156:834–837.
33. [Notes 14b]

fn14b Girgis ST, Marks GB, Downs SH, Kolbe A, Car GN, Paton R. Thunderstorm-associated asthma in an inland town in southeastern Australia. Who is at risk? Eur Respir J 2000; 16:3–8.
34. [Notes 16b]

fn16b D’Amato G, Liccardi G, Viegi G, Baldacci S. Thunderstorm-associated asthma in pollinosis patients. BMJ 2005. Available at http://bmj.bmjjournals.com/cgi/eletters/309/6947/131/c.
35. [Notes 15]

fn15 Marks GB, Colquhoun JR, Girgis ST, Koski MH, Treloar ABA, Hansen Pet al. Thunderstorm outflows preceding epidemics of asthma during spring and summer. Thorax 2001; 56:468–471.
36. [Notes 16c]

fn16c D’Amato G, Liccardi G, Viegi G, Baldacci S. Thunderstorm-associated asthma in pollinosis patients. BMJ 2005. Available at http://bmj.bmjjournals.com/cgi/eletters/309/6947/131/c.
37. [Notes 34]

fn34 D’Amato G, Ruffilli A, Ortolani C. Allergenic significance of Parietaria(pellitory-of-the-wall) pollen. In: D’AmatoG, SpieksmaF, BoniniS, editors. Allergenic pollen and pollinosis in Europe. Oxford: Blackwell Scientific Publications, 1991:113–118.
38. [Notes 23b]

fn23b Taylor PE, Hagan R, Valenta R, Glovsky MM. Release of allergens in respirable aerosols: a link between grass pollen and asthma. J Allergy Clin Immunol 2002; 109:51–56.
39. [Notes 1]

fn1 Suphioglu C, Singh MB, Taylor P, Knox RB. Mechanism of grass-pollen-induced asthma. Lancet 1992;339:569–572.
40. Antò J. Epidemic asthma. In: HolgateST, BousheyHA, FabbriLM, editors. Difficult asthma. UK: Martin Dunitz, 1999:333–340.
41. [Notes 11a]

fn11a Newson R, Strachan D, Archibald E, Emberlin J, Hardaker P, Collier C. Effect of thunderstorms and airborne grass pollen on the incidence of acute asthma in England, 1990–1994. Thorax 1997; 52:669–670.
42. [Notes 12]

fn12 Antò JM, Sunyer J. Thunderstorms: a risk factor for asthma attacks. Thorax 1997; 52:669–670.
43. [Notes 11b]

fn11b Newson R, Strachan D, Archibald E, Emberlin J, Hardaker P, Collier C. Effect of thunderstorms and airborne grass pollen on the incidence of acute asthma in England, 1990–1994. Thorax 1997; 52:669–670.
44. [Notes 35]

fn35 Antò J. Epidemic asthma. In: HolgateST, BousheyHA, FabbriLM, editors. Difficult asthma. UK: Martin Dunitz, 1999:333–340.
45. [Notes 11c]

fn11c Newson R, Strachan D, Archibald E, Emberlin J, Hardaker P, Collier C. Effect of thunderstorms and airborne grass pollen on the incidence of acute asthma in England, 1990–1994. Thorax 1997; 52:669–670.

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