Skip to main content
SpringerLink
Log in

Use of an Argentinean Wildlife Tissue Collection for Epidemiological Studies of Histoplasmosis

  • Original Article
  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

Histoplasmosis is a worldwide systemic endemic mycosis caused by several cryptic species included within the Histoplasma capsulatum complex. Domestic and wild mammals are susceptible to infection by this fungus and could be used as indicators of its presence in the environment. The aim of the study was to identify the natural reservoirs of H. capsulatum in the Argentinean Humid Pampas eco-region analyzing a wildlife frozen-tissue collection and trace its distribution patterns over time and space. Tissue samples from 34 small wild mammals caught in the Humid Pampas were analyzed using two molecular markers: 100 kDa protein coding gene (Hcp100) and ITS1 rDNA. Results showed that 32.4% of them were infected with H. capsulatum and its DNA was detected in 5/17 Calomys laucha; 3/6 Calomys musculinus; 1/5 Akodon azarae, 1/3 Monodelphis dimidiata; and 1/2 Didelphis albiventris. In the single specimen studied of Cavia aperea, no H. capsulatum DNA was detected. This is the first H. capsulatum infection report in C. laucha and C. musculinus rodents and M. dimidiate opossum which proves that tissue collections are an important source of material for epidemiological studies of endemic disease over time.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Teixeira M, Patané JSL, Taylor ML, et al. Worldwide phylogenetic distributions and population dynamics of the genus Histoplasma. PLoS Negl Trop Dis. 2016. https://doi.org/10.1371/journal.pntd.0004732.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sepúlveda VE, Márquez R, Turissini DA, Goldman WE, Matute DR. Genome sequences reveal cryptic speciation in the human pathogen Histoplasma capsulatum. mBio. 2017. https://doi.org/10.1128/mBio.01339-17.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Kauffman CA. Histoplasmosis. Clin Chest Med. 2009;30:217–25.

    PubMed  Google Scholar 

  4. Sifuentes-Osorio J, Corzo-León DE, Ponce-de-León LA. Epidemiology of invasive fungal infections in Latin America. Curr Fungal Infect Rep. 2012;6:23–34.

    Google Scholar 

  5. Negroni R, Helou SH, López-Daneri G, Robles AM, Arechavala AI, Bianchi MH. Interrupción de la profilaxis secundaria antifúngica en la histoplasmosis asociada a SIDA. Rev Iberoam Micol. 2004;21:75–8.

    PubMed  Google Scholar 

  6. Davel G, Canteros C. Situación de las micosis en la República Argentina. Rev Argent Microbiol. 2007;39:28–33.

    CAS  PubMed  Google Scholar 

  7. Riera FO, Caeiro JP, Denning DW. Burden of serious fungal infections in Argentina. J Fungi. 2018;4(2):51.

    Google Scholar 

  8. Rubinstein P, Negroni R. Histoplasmosis. Micosis Broncopulmonares del Adulto y el Niño. 2nd ed. Buenos Aires: Beta SRL; 1981. p. 249–90.

    Google Scholar 

  9. Masih D, Marticorena B, Borletto N, Farías C, Negroni R. Epidemiologic study of bronchopulmonary mycosis in the Province of Córdoba, Argentina. Rev Med Trop Sao Paulo. 1987;29:59–62.

    CAS  Google Scholar 

  10. Hoff GL, Bigler WJ. The role of bats in the propagation and spread of histoplasmosis: a review. J Wildl Dis. 1981;17:191–6.

    CAS  PubMed  Google Scholar 

  11. Constantine DG. Health precautions for bat researchers. In: Kunz TH, editor. Ecological and behavioral methods for the study of bats. London: Smithsonian Institution Press; 1988. p. 491–528.

    Google Scholar 

  12. Arias JR, Naiff RD, Naiff MF, Mok WY, Almeida MMR. Isolation of Histoplasma capsulatum from an armadillo (Dasypus novemcinctus) in the Eastern Amazon of Brazil. Trans R Soc Trop Med Hyg. 1982;76:705–6.

    CAS  PubMed  Google Scholar 

  13. Emmons CW, Ashburn LL. Histoplasmosis in wild rats; occurrence and histopathology. Public Health Rep. 1948;63(44):1416–22.

    CAS  PubMed  Google Scholar 

  14. Eisenberg T, Seeger H, Kasuga T, Eskens U, Sauerwald C, Kaim U. Detection and characterization of Histoplasma capsulatum in a German badger (Meles meles) by ITS sequencing and multilocus sequencing analysis. Med Mycol. 2013;51(4):337–44.

    CAS  PubMed  Google Scholar 

  15. Naiff RD, Mok WY, Naiff MF. Distribution of Histoplasma capsulatum in Amazonian wildlife. Mycopathologia. 1985;89(3):165–8.

    CAS  PubMed  Google Scholar 

  16. Naiff RD, Barrett TV, de Farias NM, Ferreira LC, Arias JR. New records of Histoplasma capsulatum from wild animals in the Brazilian Amazon. Rev Inst Med Trop Sao Paulo. 1996;38(4):273–7.

    CAS  PubMed  Google Scholar 

  17. Lainson R, Shaw JJ. Pneumocystis and Histoplasma infections in wild animals from the Amazon region of Brazil. Trans R Soc Trop Med Hyg. 1975;69(5–6):505–8.

    CAS  PubMed  Google Scholar 

  18. Laakkonen J, Haukisalmi V, Merritt JF. Lung parasites of shrews from Pennsylvania. J Wildl Dis. 1997;33:285–9.

    CAS  PubMed  Google Scholar 

  19. Morita T, Kishimoto M, Shimada A, Matsumoto Y, Shindo J. Disseminated histoplasmosis in a sea otter (Enhydra lutris). J Comp Pathol. 2001;125(2–3):219–23.

    CAS  PubMed  Google Scholar 

  20. Canteros CE, Iachini RH, Rivas MC, et al. Primer aislamiento de Histoplasma capsulatum de murciélago urbano Eumops bonariensis. Rev Argent Microbiol. 2005;37(1):46–56.

    CAS  PubMed  Google Scholar 

  21. Zancopé-Oliveira RM, Wanke B. Isolamento do Histoplasma capsulatum de animais silvestres no município do Rio de Janeiro. Cadernos de Saúde Pública. 1986;2(1):42–52.

    Google Scholar 

  22. Sbeghen MR, Zanata TB, Macagnan R, et al. Paracoccidioides brasiliensis infection in small wild mammals. Mycopathologia. 2015;180:435–40.

    PubMed  Google Scholar 

  23. Richini-Pereira VB, De Moraes Gimenes Bosco S, Griese J, et al. Molecular detection of Paracoccidioides brasiliensis in road-killed wild animals. Med Mycol. 2008;46(1):35–40.

    CAS  PubMed  Google Scholar 

  24. González-González AE, Ramírez JA, Aliouat-Denis CM, et al. Molecular detection of Histoplasma capsulatum in the lung of a free-ranging common noctule (Nyctalus noctula) from France using the Hcp100 gene. J Zoo Wildl Med. 2013;44(1):15–20.

    PubMed  Google Scholar 

  25. González-González AE, Aliouat-Denis CM, Ramírez-Bárcenas JA, et al. Histoplasma capsulatum and Pneumocystis spp. co-infection in wild bats from Argentina, French Guyana, and Mexico. BMC Microbiol. 2014;14:23. https://doi.org/10.1186/1471-2180-14-23.

    Article  PubMed  PubMed Central  Google Scholar 

  26. da Paz GS, Adorno BMV, Richini-Pereira VB, Bosco SMG, Langoni H. Infection by Histoplasma capsulatum, Cryptococcus spp. and Paracoccidioides brasiliensis in bats collected in urban areas. Transbound Emerg Dis. 2018;00:1–9. https://doi.org/10.1111/tbed.12955.

    Article  CAS  Google Scholar 

  27. Dos Santos B, Langoni H, Costa da Silva R, et al. Molecular detection of Histoplasma capsulatum in insectivorous and frugivorous bats in Southeastern Brazil. Med Mycol. 2017. https://doi.org/10.1093/mmy/myx138.

    Article  PubMed  Google Scholar 

  28. Toranzo AI, Tirabochi IN, Fernández N, et al. Diagnóstico molecular de histoplasmosis humana en muestras de sangre entera. Rev Argent Microbiol. 2009;41:20–6.

    CAS  PubMed  Google Scholar 

  29. Buitrago MJ, Canteros CE, Frías de León G, et al. Comparison of PCR protocols for detecting Histoplasma capsulatum DNA through a multicenter study. Rev Iberoam Micol. 2013;30(4):256–60.

    PubMed  Google Scholar 

  30. Mills JN, Ellis BA, McKee KT, et al. A longitudinal study of Junin Virus activity in the rodent reservoir of Argentine hemorrhagic fever. Am J Trop Med Hyg. 1992;47(6):749–63.

    CAS  PubMed  Google Scholar 

  31. Polop FJ, Provensal MC, Pini N, et al. Temporal and spatial host abundance and prevalence of Andes Hantavirus in Southern Argentina. EcoHealth. 2010;7:176–84.

    PubMed  Google Scholar 

  32. Bialek R, Feucht A, Aepinus C, et al. Evaluation of two nested PCR assays for detection of Histoplasma capsulatum DNA in human tissue. J Clin Microbiol. 2002;40:1644–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Kasuga T, White TJ, Koenig G, et al. Phylogeography of the fungal pathogen Histoplasma capsulatum. Mol Ecol. 2003;12(12):3383–401.

    CAS  PubMed  Google Scholar 

  34. Clothier KA, Villanueva M, Torain A, Reinl S, Barr B. Disseminated histoplasmosis in two juvenile raccoons (Procyon lotor) from a nonendemic region of the United States. J Vet Diagn Investig. 2014;26:297–301.

    Google Scholar 

  35. Burek-Huntington KA, Gill V, Bradway DS. Locally acquired disseminated histoplasmosis in a northern sea otter (Enhydra lutris kenyoni) in Alaska, USA. J Wildl Dis. 2014;50(2):389–92.

    PubMed  Google Scholar 

  36. Leading International Fungal Education (LIFE). Skin testing for endemic fungi. https://life-worldwide.org/en/skin-testing-endemic. Accessed 16 Feb 2018.

  37. Dunnum J, Zeballos H, Vargas J et al. Cavia aperea. The IUCN Red list of threatened species 2008. https://doi.org/10.2305/iucn.uk.2008.rlts.t4064a10346778.en. Accessed 16 Feb 2018.

  38. Sanches VQA, Gomes MMA, Passos FC, Graciolli G, Ribas ACA. Home-range and space use by Didelphis albiventris (Lund 1840) (Marsupialia, Didelphidae) in Mutum Island, Paraná river, Brazil. Biota Neotrop. 2012;12(4):50–5.

    Google Scholar 

  39. Steinmann AR, Priotto JW, Castillo EA, Polop JJ. Size and overlap of home range in Calomys musculinus (Muridae: Sigmodontinae). Acta Theriol. 2005;50(2):197–206.

    Google Scholar 

  40. Taylor ML, Chávez-Tapia CB, Vargas-Yañez R, et al. Environmental conditions favoring bat infection with Histoplasma capsulatum in Mexican shelters. Am J Trop Med Hyg. 1999;61(6):914–9.

    CAS  PubMed  Google Scholar 

  41. Silva-Vergara ML, Martinez R, Borges-Malta ME, Leite-Maffei CM, Ramirez LE. Histoplasma capsulatum isolated from Didelphis albiventris (Marsupialia: Didelphidae) in the State of Minas Gerais, Brazil. Rev Iberoam Micol. 2001;18(4):180–2.

    CAS  PubMed  Google Scholar 

  42. Taylor RL, Shacklette MH. Naturally acquired histoplasmosis in the mammals of the Panama Canal Zone. Am J Trop Med Hyg. 1962;11:796–9.

    CAS  PubMed  Google Scholar 

  43. López LF, Muñoz CO, Cáceres DH, Tobón ÁM, Loparev V, Clay O, Chiller T, Litvintseva A, Gade L, González Á, Gómez BL. Standardization and validation of real time PCR assays for the diagnosis of histoplasmosis using three molecular targets in an animal model. PLoS ONE. 2017. https://doi.org/10.1371/journal.pone.0190311.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Kim TH, Han JH, Chang SN, et al. Adiaspiromycosis of an Apodemus agrarius captured wild rodent in Korea. Lab Anim Res. 2012;28(1):67–9.

    PubMed  PubMed Central  Google Scholar 

  45. Borman AM, Simpson VR, Palmer MD, Linton CJ, Johnson EM. Adiaspiromycosis due to Emmonsia crescens is widespread in native British mammals. Mycopathologia. 2009;168(4):153–63.

    PubMed  Google Scholar 

  46. Albassam MA, Bhatnagar R, Lillie LE, Roy L. Adiaspiromycosis in striped skunks in Alberta, Canada. J Wildl Dis. 1986;22(1):13–8.

    CAS  PubMed  Google Scholar 

  47. Hubalek Z. Emmonsiosis of wild rodents and insectivores in Czechland. J Wildl Dis. 1999;35:243–9.

    CAS  PubMed  Google Scholar 

  48. Sahaza J, Suárez-Alvarez R, Estrada-Bárcenas D, Pérez-Torres A, Taylor ML. Profile of cytokines in the lungs of BALB/c mice after intra-nasal infection with Histoplasma capsulatum mycelial propagules. Comp Immunol Microbiol Infect Dis. 2015;41:1–9.

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the support of the professionals and technicians of the tissues Collection of the National Institute of Human Viral Diseases INEVH-ANLIS “Dr. Julio I. Maiztegui” in obtaining the tissue samples for this work.

Author information

Authors and Affiliations

  1. Servicio Micosis Profundas, Departamento Micología, Instituto Nacional de Enfermedades Infecciosas INEI-ANLIS “Dr. Carlos G. Malbrán”, Av. Vélez Sarsfield 563, C1282AFF, Ciudad Autónoma de Buenos Aires, Argentina

    Cristina E. Canteros, Adriana I. Toranzo, Héctor D. Salas, María C. López-Joffre & Roberto Osvaldo Suárez-Alvarez

  2. Departamento Investigación, Instituto Nacional de Enfermedades Virales Humanas INEVH-ANLIS “Dr. Julio I. Maiztegui”, Monteagudo 2510, B2700, Pergamino, Provincia de Buenos Aires, Argentina

    Silvana Levis

Authors
  1. Cristina E. Canteros
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adriana I. Toranzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Silvana Levis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Héctor D. Salas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. María C. López-Joffre
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Roberto Osvaldo Suárez-Alvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Roberto Osvaldo Suárez-Alvarez.

Ethics declarations

Conflict of interest

The authors have seen and approved the final version of the manuscript and declare that there is no potential, personal, academic, financial or intellectual conflict of interest among them.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling Editor: Mario Augusto Ono.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Canteros, C.E., Toranzo, A.I., Levis, S. et al. Use of an Argentinean Wildlife Tissue Collection for Epidemiological Studies of Histoplasmosis. Mycopathologia 185, 905–915 (2020). https://doi.org/10.1007/s11046-020-00430-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-020-00430-3

Keywords

Search

Navigation