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Adiaspiromycosis and Diseases Caused by Related Fungi in Ajellomycetaceae

  • Andrew M. Borman
  • Yanping Jiang
  • Karolina Dukik
  • Lynne Sigler
  • Ilan S. Schwartz
  • G. Sybren de Hoog
Chapter

Abstract

Adiaspiromycosis, classically caused by Emmonsia species, is primarily a pulmonary disease affecting small mammals, especially members of the orders Rodentia and Carnivora. The disease name derives from the tissue form of the fungus (adiaspores), which develops when the inhaled conidia of the mycelial form of the fungus present in soil enlarge in lungs to produce thick-walled non-replicative structures. Emmonsia crescens has apparently worldwide distribution and is associated with very large adiaspores (up to 400 μm). The type species of Emmonsia, E. parva, however, is now recognised to be a Blastomyces species and its ‘small adiaspores’ are comparable to the broad-based budding cells current in that genus. This chapter briefly summarises current knowledge concerning taxonomy, epidemiology, biology and clinical syndromes of the principal etiological agents of adiaspiromycosis in mammals.

Keywords

Adiaspiromyces crescens Emmonsia parva Adiaspiromycosis Mammals Zoonoses Adiaspores 

References

  1. Albassam MA, Bhatnagar R, Lillie LE, Roy L (1986) Adiaspiromycosis in striped skunks in Alberta, Canada. J Wildl Dis 22:13–18CrossRefPubMedGoogle Scholar
  2. Anstead GM, Sutton DA, Graybill JR (2012) Adiaspiromycosis causing respiratory failure and a review of human infections due to Emmonsia and Chrysosporium spp. J Clin Microbiol 50:1346–1354CrossRefPubMedPubMedCentralGoogle Scholar
  3. Austwick PKC (1968) Mycotic infections. Symp Zool Soc Lond 24:249–271Google Scholar
  4. Barbas Filho JV, Amato MB, Deheinzelin D, Saldiva PH, de Carvalho CR (1990) Respiratory failure caused by adiaspiromycosis. Chest 97:1171–1175CrossRefPubMedGoogle Scholar
  5. Boisseau-Lebreuil HT (1975) In vitro formation of adiaspores in 10 strains of Emmonsia crescens, the fungal agent of adiaspiromycosis. CR Séances Soc Biol Fil 169:1057–1061Google Scholar
  6. Borman AM, Simpson VR, Palmer MD, Linton CJ, Johnson EM (2009) Adiaspiromycosis due to Emmonsia crescens is widespread in native British mammals. Mycopathologia 68:153–163CrossRefGoogle Scholar
  7. Buyuksirin M, Ozkayaa S, Yucel N, Guldaval F, Ceylan K, Erbay Polat G (2011) Pulmonary adiaspiromycosis: the first reported case in Turkey. Respir Med CME 4:166–169CrossRefGoogle Scholar
  8. Chantrey JC, Borman AM, Johnson EM, Kipar A (2006) Emmonsia crescens infection in a British water vole (Arvicola terrestris). Med Mycol 44:375–378CrossRefPubMedGoogle Scholar
  9. Ciferri R, Montemartini A (1959) Taxonomy of Haplosporangium parvum. Mycopathologia 10:303–316Google Scholar
  10. Cronje N, Schwartz IS, Retief L et al (2017) Attempted molecular detection of the dimorphic fungal pathogen, Emergomyces africanus, in small terrestrial mammals in South Africa. Med Mycol.  https://doi.org/10.1093/mmy/myx065
  11. de Almeida Barbosa A, Moreira Lemos AC, Severo LC (1997) Acute pulmonary adiaspiromycosis. Report of three cases and a review of 16 other cases collected from the literature. Rev Iberoam Micol 14:177–180PubMedGoogle Scholar
  12. de Hoog GS, Redhead SA, Feng P, Jiang Y, Dukik K, Sigler L (2017) Proposals to conserve Blastomyces Gilchrist & W.R. Stokes against Blastomyces Costantin & Rolland and Ajellomycetaceae against Paracoccidioidaceae (Ascomycota: Onygenales). Taxon 65:1167–1169CrossRefGoogle Scholar
  13. Denson JL, Keen CE, Froeschle PO, Toy EW, Borman AM (2009) Adiaspiromycosis mimicking widespread malignancy in a patient with pulmonary adenocarcinoma. J Clin Pathol 62:837–839CrossRefPubMedGoogle Scholar
  14. Doby JM, Boisseau-Lebreuil MT, Rault B (1971) L’adiaspiromycose par Emmonsia crescens chez les petits mammiferes sauvages en France. Mycopathologia 44:107–115Google Scholar
  15. Doby-Dubois M, Chevrel ML, Doby JM, Louvet M (1964) Premier cas humain d’adiaspiromycose par Emmonsia crescens, Emmons et Jellison 1960. Bull Soc Pathol Exot 57:240–244Google Scholar
  16. Dot J-M, Debourgogne A, Champigneulle J, Salles Y, Brizion M, Puyhardy JM, Collomb J, Plénat F, Machouart M (2009) Molecular diagnosis of disseminated adiaspiromycosis due to Emmonsia crescens. J Clin Microbiol 47:1269–1273CrossRefPubMedPubMedCentralGoogle Scholar
  17. Drouhet E, Guého E, Gori S, Huerre M, Provost F, Borgers M, Dupont B (1998) Mycological, ultrastructural and experimental aspects of a new dimorphic fungus Emmonsia pasteuriana sp. nov. isolated from a cutaneous disseminated mycosis in AIDS. J Mycol Med 8:64–77Google Scholar
  18. Dukik K, Muñoz JF, Jiang Y, Feng P, Sigler L, Stielow JB et al (2017) Novel taxa of thermally dimorphic systemic pathogens in the Ajellomycetaceae (Onygenales). Mycoses 60:296–309CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dvořák J, Otcenášek M, Prokopič J (1969) The spring peak of adiaspiromycosis due to Emmonsia crescens Emmons and Jellison 1960. Sabouraudia 7:12–14CrossRefPubMedGoogle Scholar
  20. Dvořák J, Otcenášek M, Rosicky B (1973) Adiaspiromycosis caused by Emmonsia crescens Emmons and Jellison 1960. Studie CSAV c14. Academia Press, PragueGoogle Scholar
  21. Echavarria E, Cano EL, Restrepo A (1993) Disseminated adiaspiromycosis in a patient with AIDS. J Med Vet Mycol 31:91–97CrossRefPubMedGoogle Scholar
  22. Emmons CW, Jellison WL (1960) Emmonsia crescens sp. nov. and adiaspiromycosis (haplomycosis) in mammals. Ann N Y Acad Sci 89:91–101CrossRefPubMedGoogle Scholar
  23. England DM, Hochholzer L (1993) Adiaspiromycosis: an unusual fungal infection of the lung. Report of 11 cases. Am J Surg Pathol 17:876–886CrossRefPubMedGoogle Scholar
  24. Feng P, Yin S, Zhu G et al (2015) Disseminated infection caused by Emmonsia pasteuriana in a renal transplant recipient. J Dermatol 42:1179–1182CrossRefPubMedGoogle Scholar
  25. Gori S, Drouhet E (1998) Cutaneous disseminated mycosis in a patient with AIDS due to a new dimorphic fungus. J Mycol Med 8:57–63Google Scholar
  26. Hubalek Z (1999) Emmonsiosis of wild rodents and insectivores in Czechland. J Wildl Dis 35:243–249CrossRefPubMedGoogle Scholar
  27. Hubalek Z, Nesvadboda J, Rychnovsky B (1995) A heterogeneous distribution of Emmonsia parva var. crescens in an agro-system. J Med Vet Mycol 33:197–200CrossRefPubMedGoogle Scholar
  28. Hubalek Z, Zejda J, Svobodová Š, Kuĉera J (1993) Seasonality of rodent adiaspiromycosis in a lowland forest. J Med Vet Mycol 31:359–366CrossRefGoogle Scholar
  29. Hubalek Z, Burda H, Scharff A, Heth G, Nevo E, Sumbera R, Pesko J, Zima J (2005) Emmonsiosis of subterranean rodents (Bathyergidae, Spalacidae) in Africa and Israel. Med Mycol 43(8):691–697CrossRefPubMedGoogle Scholar
  30. Jellison WL (1969) Adiaspiromycosis (=haplomycosis). Mountain Press, MontanaGoogle Scholar
  31. Jellison WL, Helminen M, Vinson JW (1960) Presence of a pulmonary fungus in rodents in Finland. Ann Med Exp Fenn 38:3–8Google Scholar
  32. Jiang Y, Dukik K, Muñoz J, Sigler L, Schwartz IS et al (2018) Phylogeny, ecology and taxonomy of systemic pathogens in Ajellomycetaceae (Onygenales). Fungal Divers (in press)Google Scholar
  33. Kenyon C, Corcoran C, Govender NP (2014) An Emmonsia species causing disseminated infection in South Africa. N Engl J Med 370:283–284CrossRefGoogle Scholar
  34. Krivanec K (1977) Adiaspiromycosis in Czechoslovakian mammals. Sabouraudia 15:221–223CrossRefPubMedGoogle Scholar
  35. Krivanec K, Otcenasek M (1977) Importance of free living mustelid carnivores in circulation of adiaspiromycosis. Mycopathologia 60:139–144CrossRefPubMedGoogle Scholar
  36. Krivanec K, Octenasek M, Rosicky B (1975) The role of polecats of the genus Putorius Cuvier, 1987 in natural foci of adiaspiromycosis. Folia Parasitol 22:245–249PubMedGoogle Scholar
  37. Krivanec K, Otcenasek M, Slais J (1976) Adiaspiromycosis in large free-living carnivores. Mycopathologia 58:21–25CrossRefPubMedGoogle Scholar
  38. Kodousek R (1972) Finding of isolated spherules of the fungus Emmonsia crescens in surgical specimen of the appendix in a 7-year-old boy. Cesk Patol 8:160–162PubMedGoogle Scholar
  39. Kodousek R, Vortel V, Fingerland A (1971) Pulmonary adiaspiromycosis in man caused by Emmonsia crescens: report of a unique case. Am J Clin Pathol 56:394–399CrossRefPubMedGoogle Scholar
  40. Leighton FA, Wobeser G (1978) The prevalence of adiaspiromycosis in three sympatric species of ground squirrels. J Wildl Dis 14:362–365CrossRefPubMedGoogle Scholar
  41. Li RK, Ciblak MA, Nordoff N, Pasarell L et al (2000) In vitro activities of voriconazole, itraconazole, and amphotericin B against Blastomyces dermatitidis, Coccidioides immitis, and Histoplasma capsulatum. Antimicrob Agents Chemother 44(6):1734–1736CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lugton IW, Wobeser G, Morris RS, Caley P (1997) Epidemiology of Mycobacterium bovis in feral ferrets (Mustela furo) in New Zealand. N Z Vet J 45:140–150CrossRefPubMedGoogle Scholar
  43. Malik R, Capoor MR, Vanidassane I et al (2016) Disseminated Emmonsia pasteuriana infection in India: a case report and a review. Mycoses 59:127–132CrossRefPubMedGoogle Scholar
  44. Martins RL, Santos CG, França FR, Moraes MA (1997) Human adiaspiromycosis. A report of a case treated with ketoconazole. Rev Soc Bras Med Trop 30:507–509CrossRefPubMedGoogle Scholar
  45. Mason R, Gauhwin M (1982) Adiaspiromycosis in south Australian hairy-nosed wombats (Lasiorhinus latifrons). J Wildl Dis 18:3–8CrossRefPubMedGoogle Scholar
  46. McDiarmid A, Austwick PK (1954) Occurrence of Haplosporangium parvum in the lungs of the mole (Talpa europaea). Nature 174:843–844CrossRefPubMedGoogle Scholar
  47. Mendes MO, Moraes MA, Renoiner EI, Dantas MH, Lanzieri TM, Fonseca CF, Luna EJ, Hatch DL (2009) Acute conjunctivitis with episcleritis and anterior uveitis linked to adiaspiromycosis and freshwater sponges, Amazon region, Brazil, 2005. Emerg Infect Dis 15:633–639CrossRefPubMedPubMedCentralGoogle Scholar
  48. Moraes MA, Gomes MI (2004) Human adiaspiromycosis: cicatricial lesions in mediastinal lymph nodes. Rev Soc Bras Med Trop 37:177–178CrossRefPubMedGoogle Scholar
  49. Nuorva K, Pitkänen R, Issakainen J, Huttunen NP, Juhola M (1997) Pulmonary adiaspiromycosis in a two year old girl. J Clin Pathol 50:82–85CrossRefPubMedPubMedCentralGoogle Scholar
  50. Pelegrin I, Ayats J, Xiol X, Cuenca-Estrella M et al (2011) Disseminated adiaspiromycosis: case report of a liver transplant patient with human immunodeficiency infection, and literature review. Transpl Infect Dis 13(5):507–514CrossRefPubMedGoogle Scholar
  51. Peres LC, Figueiredo F, Peinado M, Soares FA (1992) Fulminant disseminated pulmonary adiaspiromycosis in humans. Am J Trop Med Hyg 46:146–150CrossRefPubMedGoogle Scholar
  52. Peterson SW, Sigler L (1998) Molecular genetic variation in Emmonsia crescens and Emmonsia parva, etiologic agents of adiaspiromycosis, and their phylogenetic relationship to Blastomyces dermatitidis (Ajellomyces dermatitidis) and other systemic fungal pathogens. J Clin Microbiol 36:2918–2925PubMedPubMedCentralGoogle Scholar
  53. dos Santos VM, Fatureto MC, Saldanha JC, Adad SJ (2000) Pulmonary adiaspiromycosis: report of two cases. Rev Soc Bras Med Trop 33:483–488CrossRefPubMedGoogle Scholar
  54. Schwartz IS, Govender NP, Corcoran C et al (2015a) Clinical characteristics, diagnosis, management and outcomes of disseminated emmonsiosis: a retrospective case series. Clin Infect Dis 61:1004–1012CrossRefPubMedGoogle Scholar
  55. Schwartz IS, Kenyon C, Feng P et al (2015b) 50 years of Emmonsia disease in humans: the dramatic emergence of a cluster of novel fungal pathogens. PLoS Pathog 11:e100e5198CrossRefGoogle Scholar
  56. Schwartz IS, Lerm B, Hoving JC et al (2018a) Emergomyces africanus in soil, South Africa. Emerg Infect Dis 24(2):377–380.  https://doi.org/10.3201/eid2402.171351CrossRefPubMedPubMedCentralGoogle Scholar
  57. Schwartz IS, McLoud JD, Berman D et al (2018b) Molecular detection of airborne Emergomyces africanus, a thermally dimorphic fungal pathogen, in Cape Town, South Africa. PLoS Negl Trop Dis 12(1):e0006174.  https://doi.org/10.1371/journal.pntd.0006174CrossRefPubMedPubMedCentralGoogle Scholar
  58. Sharapov VM (1969) Adiaspiromycosis in the U.S.S.R. Izv Sibirsk Otdel AN SSSR Ser Biol-Med Nauk 1:86–95Google Scholar
  59. Severo LC, Geyer GR, Camargo JJ, Porto NS (1989) Adiaspiromycosis treated successfully with ketoconazole. J Med Vet Mycol 27:265–268CrossRefPubMedGoogle Scholar
  60. Sigler L (1996) Ajellomyces crescens sp. nov.: taxonomy of Emmonsia species and relatedness with Blastomyces dermatitidis (teleomorph Ajellomyces dermatitidis). J Med Vet Mycol 34:303–314CrossRefPubMedGoogle Scholar
  61. Sigler L (2005) Adiaspiromycosis and other infections caused by Emmonsia species. In: Merz WG, Hay RJ (eds) Medical mycology, Topley and Wilson’s microbiology and microbial infections, 10th edn. Hodder Arnold Press, London, pp 809–824Google Scholar
  62. Sigler L, Flis A (1998) Catalogue of the University of Alberta Microfungus Collection and Herbarium. University of Alberta Devonian Botanic Garden, Edmonton, pp 1–213Google Scholar
  63. Silva RM, Liporoni GA, Botto CC, Rodrigues BC, Scudeler D, Cunha Junior W (2010) Pulmonary adiaspiromycosis treated without antifungal drugs. Rev Soc Bras Med Trop 43:95–97CrossRefPubMedGoogle Scholar
  64. Simpson VR, Gavier-Wilden D (2000) Fatal adiaspiromycosis in a wild Eurasian otter (Lutra lutra). Vet Rec 147:239–241CrossRefPubMedGoogle Scholar
  65. Tang XH, Zhou H, Zhang XQ, Han JD, Gao Q (2015) Cutaneous disseminated emmonsiosis due to Emmonsia pasteuriana in a patient with cytomegalovirus enteritis. JAMA Dermatol 151:1026–1028CrossRefGoogle Scholar
  66. Tevis L (1956) Additional records of Haplosporangium parvum in mammals in Britain. Nature 177:437CrossRefGoogle Scholar
  67. Turner D, Burke M, Bashe E, Blinder S, Yust I (1999) Pulmonary adiaspiromycosis in a patient with acquired immunodeficiency syndrome. Eur J Clin Microbiol Infect Dis 18:893–895CrossRefPubMedGoogle Scholar
  68. Wang P, Kenyon C, de Hoog S, Guo L, Fan H, Liu H, Li Z, Sheng R, Yang Y, Jiang Y, Zhang L, Xu Y (2017) A novel dimorphic pathogen, Emergomyces orientalis (Onygenales), agent of disseminated infection. Mycoses 60:310–319CrossRefPubMedGoogle Scholar
  69. Watts JC, Chandler FW (1975) Human pulmonary adiaspiromycosis. Arch Pathol 99:11–15PubMedGoogle Scholar
  70. Wheat LJ, Freifeld AG, Kleiman MB, Baddley JW, McKinsey DS, Loyd JE, Kauffman CA, Infectious Diseases Society of America (2007) Clinical practice guidelines for the management of patients with histoplasmosis: 2007 update by the Infectious Diseases Society of America. Clin Infect Dis 45:807–825CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Andrew M. Borman
    • 1
  • Yanping Jiang
    • 2
    • 3
  • Karolina Dukik
    • 4
  • Lynne Sigler
    • 5
  • Ilan S. Schwartz
    • 6
  • G. Sybren de Hoog
    • 3
    • 4
  1. 1.UK National Mycology Reference Laboratory, Public Health EnglandBristolUK
  2. 2.Department of DermatologyThe Affiliated Hospital, Guizhou Medical UniversityGuiyangChina
  3. 3.Center of Expertise in Mycology Radboudumc/CWZNijmegenThe Netherlands
  4. 4.Westerdijk Fungal Biodiversity InstituteUtrechtThe Netherlands
  5. 5.Microfungus Collection and Herbarium [now UAMH Centre for Global Microfungal Diversity] and Biological SciencesUniversity of AlbertaEdmontonCanada
  6. 6.Division of Infectious Diseases, Department of MedicineUniversity of AlbertaEdmontonCanada

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