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Aspergillosis in the USA, UK, and Japan in the 20th Century

Explore the history and understanding of Aspergillosis in the USA, UK, and Japan in the 20th century, including the discovery of different species and the classification of the disease. Learn about the impact of airborne fungi on asthma and the development of allergic bronchopulmonary aspergillosis.

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Aspergillosis in the USA, UK, and Japan in the 20th Century

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  1. Aspergillosis in the USA, UK, and Japan in the 20th Century David W. Denning Wythenshawe Hospital University of Manchester With many thanks to Aya Homei

  2. In 1901 • UK - Queen Victoria died, Boer war in South Africa, Boxer rebellion in China allowed an open door trade policy, Hong Kong 99 year lease, rise of socialism (Fabian Society).

  3. In 1901 • US – McKinley assassinated and succeeded by Roosevelt, rise of big business and anti-Trust sentiment, war with Spain forced Cuba to be independent, annexed Hawaii, Guam, Philippines and Puerto Rica

  4. In 1901 • Japan – under Emperor Matsuhito, post Sino-Japanese war controlled part of China (natural resources), Korea, Taiwan, transformation to an industrial economy with ‘democratic’ parliament

  5. And what did we know about Aspergillus in 1901? Many species had been described including:A. flavus – Link, 1809A. fumigatus – Fresnius, 1863A. niger - v. Tiegham, 1867A. nidulans - (Eidam) Winter, 1884

  6. A. fumigatus by JB Georg W Fresnius Isolates obtained from human lung tissue. Isolates obtained from the bronchi and the lung of a bustard, Fresnius, Beiträge zur Mykologie, 1863

  7. And what did we know about aspergillosis? Aspergillomas known (Bennett, 1842), but not described as such Wheezing and coughing in wig combers and pigeon crammers (Popoff, 1887; Renon 1897) Superficial aspergillosis described (otomycosis by Mayer, 1844; keratitis by Leber 1879) Sinus aspergillosis described (maxillary by Zarniko, 1891; sphenoid by Oppe, 1897) Few cases of invasive aspergillosis in normal hosts (pleural by Rayer, 1842 and renal by Ross in 1891)

  8. Aspergillus tracheobronchitis - 1890 Autopsy drawing of a ‘normal’ 3 year old who died over 10 days Wheaton Path Trans 1890; 41:34-37

  9. Remarks upon a case of aspergillar mycosis- 1893 Boyce R, Journal of Pathology and Bacteriology1893;1:163-6.

  10. Invasive aspergillosis • Acute (<1 month course) • Subacute/chronic necrotising (1-3 months) Chronic aspergillosis (>3 months) • Chronic cavitary pulmonary • Aspergilloma of lung • Chronic fibrosing pulmonary • Chronic invasive sinusitis • Maxillary (sinus) aspergilloma Allergic • Allergic bronchopulmonary (ABPA) • Extrinsic allergic (broncho)alveolitis (EAA) • Asthma with fungal sensitisation (SAFS) • Allergic Aspergillus sinusitis (eosinophilic fungal rhinosinusitis) CLASSIFICATION OF ASPERGILLOSIS Airways/nasal exposure to airborne Aspergillus

  11. Invasive aspergillosis • Acute (<1 month course) • Subacute/chronic necrotising (1-3 months) Chronic aspergillosis (>3 months) • Chronic cavitary pulmonary • Aspergilloma of lung • Chronic fibrosing pulmonary • Chronic invasive sinusitis • Maxillary (sinus) aspergilloma Allergic • Allergic bronchopulmonary (ABPA) • Extrinsic allergic (broncho)alveolitis (EAA) • Asthma with fungal sensitisation (SAFS) • Allergic Aspergillus sinusitis (eosinophilic fungal rhinosinusitis) CLASSIFICATION OF ASPERGILLOSIS Airways/nasal exposure to airborne Aspergillus

  12. Asthma and airborne fungi 1870’s - exacerbation of asthma by airborne fungi – Charles Blackley (Manchester physician) 1920’s - Cadham reported exacerbation of asthma by wheat rust - van Leeuwen reported relief of asthma with filtered air and mould skin test +ve’s in >50% of asthmatics Denning et al, Eur Resp J 2006 In press

  13. Fungi in housedust

  14. Asthma and airborne fungi 1870’s - exacerbation of asthma by airborne fungi – Charles Blackley (Manchester physician) 1920’s - Cadham reported exacerbation of asthma by wheat rust - van Leeuwen reported relief of asthma with filtered air and mould skin test +ve’s in >50% of asthmatics - Jiminez- Diaz reported climatic asthma (mostly related to moulds) - Cohen showed removal of house dust antigen in furniture helped mould skin test +ve asthmatics Denning et al, Eur Resp J 2006 In press

  15. Asthma and airborne fungi 1870’s - exacerbation of asthma by airborne fungi – Charles Blackley (Manchester physician) 1920’s - Cadham reported exacerbation of asthma by wheat rust - van Leeuwen reported relief of asthma with filtered air and mould skin test +ve’s in >50% of asthmatics - Jiminez- Diaz reported climatic asthma (mostly related to moulds) - Cohen showed removal of house dust antigen in furniture helped mould skin test +ve asthmatics 1930’s – Asthma related to Alternaria, Trichophyton and A. fumigatus - sc A. fumigatus skin test (1:5000 extract) exacerbated asthma Denning et al, Eur Resp J 2006 In press

  16. Experimental aspergillosis “The mold, Aspergillus fumigatus, is a cause of spontaneous infections in man, domestic animals, and both domestic and wild birds. In man and the mammals such infections are so rare as to be of little practical importance.. .. ..” Henrici. J Immunol 1939;36:319

  17. Allergic bronchopulmonary aspergillosis - 1952 • First full description of ABPA • complication of asthma • coughing up casts • episodes of ‘pneumonia’/ mucous impaction • skin test positive for Aspergillus Hinson, Moon & Plummer. Thorax 1952:7:317

  18. Aspergillus precipitins – early 1960’s • fumigatus • A. flavus • A. nidulans Longbottom, Pepys and Temple Clive. Lancet 1964;i:588

  19. IgE testing and routine intradermal skin prick testing Skin test and precipitin reactions to A. fumigatus Pepys. Am Rev Resp Dis 1964;90:465-7

  20. Open trial of itraconazole in ABPA - 1991 BeforeAfter Prednisone (mg/d) 43 24* Total IgE 2462 525* FEV1 1.48 1.79* FVC 2.3 2.9 *p=0.04 Only 1 patient failed – he had low itraconazole levels. Denning et al, Chest 1991; 35:1329

  21. Randomised trial of itraconazole in ABPA - 2000 ItraPlacebo Phase 1 Overall response 13/28 (46%) 5/27 (19%) p=0.04 Age >50 8/12 (67%) 3/14 (21%) p=0.045 Stevens et al, New Engl J Med 2000; 342:756

  22. CLASSIFICATION OF ASPERGILLOSIS Invasive aspergillosis • Acute (<1 month course) • Subacute/chronic necrotising (1-3 months) Airways/nasal exposure to airborne Aspergillus Chronic aspergillosis (>3 months) • Chronic cavitary pulmonary • Aspergilloma of lung • Chronic fibrosing pulmonary • Chronic invasive sinusitis • Maxillary (sinus) aspergilloma Allergic • Allergic bronchopulmonary (ABPA) • Extrinsic allergic (broncho)alveolitis (EAA) • Asthma with fungal sensitisation • Allergic Aspergillus sinusitis (eosinophilic fungal rhinosinusitis)

  23. Radiology of aspergilloma Fukushima K & Sassa R. Clinical aspects of aspergillosis. Japan. J. Med. Mycol. 1, 1960: 19.

  24. Pathology of aspergilloma Fukushima K & Sassa R. Clinical aspects of aspergillosis. Japan. J. Med. Mycol. 1, 1960: 19.

  25. Aspergillus precipitins Severo on www.aspergillus.man.ac.uk

  26. Skin test and precipitin reactions to A. fumigatus Pepys. Am Rev Resp Dis 1964;90:465-7

  27. Simple (single) aspergilloma Patient RT December 2002 Cough (mild) & tired Wythenshawe Hospital

  28. Aspergilloma Severo on www.aspergillus.man.ac.uk

  29. Surgery for aspergilloma Early experiences were: 14 resections: 8 lobectomies, 3 pneumonectomies and 4 segemental resections No problems = 7 Space problems = 5 (+2 empyema) thoracoplasty = 3 Death = 2 (resp failure) Kilman et al J Cardiovasc Surg 1969;57:642

  30. Bilateral fibrocystic sarcoidosis with bilateral asperillomas Wythenshawe Hospital

  31. Sarcoidosis and aspergilloma 3 cases among 122 patients with sarcoid [Retrospective] [Prospective] 12 among 100 patients screened with Aspergillus precipitins, 10 had aspergillomas (10% rate) 19 had stage III (cystic parenchymal disease) and all 10 aspergillomas were in these patients (50% rate). Winterbauer & Kraemer, Ar Intern Med 1976;136:1356. Wollschalger & Khan. Chest 1984;86:585

  32. CLASSIFICATION OF ASPERGILLOSIS Invasive aspergillosis • Acute (<1 month course) • Subacute/chronic necrotising (1-3 months) Airways/nasal exposure to airborne Aspergillus Chronic aspergillosis (>3 months) • Chronic cavitary pulmonary • Aspergilloma of lung • Chronic fibrosing pulmonary • Chronic invasive sinusitis • Maxillary (sinus) aspergilloma Allergic • Allergic bronchopulmonary (ABPA) • Extrinsic allergic (broncho)alveolitis (EAA) • Asthma with fungal sensitisation • Allergic Aspergillus sinusitis (eosinophilic fungal rhinosinusitis)

  33. Invasive aspergillosis as an opportunistic infection - 1953 Rankin. Br Med J 1953;1(April 25th):918

  34. Invasive aspergillosis as an opportunistic infection - 1953 • First description in Gloucester, UK • 45 year window cleaner, thigh abscess • complication of pancytopenia as a result of chloramphenicol toxicity • autopsy diagnosis of disseminated aspergillosis, with vascular invasion, together with ‘moniliasis’ Rankin. Br Med J 1953;1(April 25th):918

  35. Eniwetok atoll in Marshall Islands 200 miles west of Bikini atoll –1st H bomb test 1st November 1952

  36. Bikini atoll - Marshall Islands 2nd H bomb test 1st March 1954

  37. Operation Castle at Bikini atoll - Bravo

  38. Fishing boat Lucky Dragon was caught in the blast and it rained.All crew members were exposedMr Aikichi Kuboyama, the radio operator was most affected by radiation sickness

  39. Invasive aspergillosis complicating radiation sickness presented in 1st Tokyo National Hospital - 1954. Mr Aikichi Kuboyama died after 207 days in hospital on Sept 23rd 1954. Autopsy showed “A. fumigatus infection and concomitant pneumonic lesion of the upper right and lower left pulmonary lobes” Okudaira. Acta Pathologica Japonica 1955;5:117-24.

  40. Professor Okudaira presented the case to senior mycologists at the ‘Research Committee of Hyphomycoses’ Aya Homei, taken on November 12, 2006

  41. Sake manufacture Ancient woodcut from Japan

  42. Postgraduate education and awareness Yamashita. The first step to the identification of the Aspergilli. Japan J Med Mycol 1, 1960: 213.

  43. Lucky Dragon (Daigo Fukuryumaru) Exhibition Hall Aya Homei, personal collection

  44. Foyer of the Lucky Dragon exhibition Aya Homei, personal collection

  45. The Lucky Dragon itself Aya Homei, personal collection

  46. The Lucky Dragon itself Aya Homei, personal collection

  47. Postcard from the Lucky Dragon Exhibition Hall Aya Homei, personal collection

  48. Increasing invasive aspergillosis in Japan in 1980’s 1969 1980 1990 1994 Yamazaki et al, J Clin Microbiol 1999;37:1732

  49. Fraser et al, JAMA 1979;242:1631

  50. Change from 1970 to 1976 in projected incidence (cases per 1 million per year) of systemic mycoses requiring hospitalisation +180 4.8 +160 1976 rate +140 +120 1970 rate +100 3.2 2.3 +80 17.9 +60 Blastomycosis Sporotrichosis % change +40 23.0 +20 1.8 0.2 0.5 0 19.7 10.3 1.9 1.7 1.3 1.7 0.6 -20 -40 Candidiasis Aspergillosis Actinomycosis Cryptococcosis Histoplasmosis -60 Coccidioidomycosis -80 0.9 -100 Fraser et al, JAMA 1979;242:1631

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