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Comparative Clinical Pathology

, Volume 28, Issue 1, pp 263–269 | Cite as

Pathology and molecular diagnosis of histoplasmosis in a captive green monkey (Chlorocebus sabaeus) in Ibadan, Nigeria

  • O. O. Alaka
  • O. A. Fagbohun
  • T. A. Jarikre
  • V. O. Oyebanji
  • R. D. Adesina
  • W. U. Anike
  • B. C. Okpe
  • R. E. Antia
  • Benjamin O. EmikpeEmail author
  • S. O. Akpavie
Case Report
  • 6 Downloads

Abstract

An adult green monkey (Chlorocebus sabaeus) donated to the zoological garden after history of attack on the owner about a year earlier was found dead a week later with history of sluggish reflexes. At necropsy, there was severe adhesive pleuritis, multifocal to coalescing broncho-interstitial granulomatous pneumonia, diffuse granulomatous splenitis, unilateral multifocal granulomatous epididymitis, and orchitis with moderately congested meningeal blood vessels and shrunken sulci. Histological examination of all tissues stained with routine Hematoxylin and Eosin, Periodic Acid Schiff, and Grocott’s methenamine silver stains showed numerous intrahistiocytic (macrophages and giant cells) and extracellular round (10–30 μm) yeast with double-contoured refractile wall. The yeasts exhibited broad-based budding in some tissues. Molecular detection of the 18S rDNA gene of the fungus was amplified from the extracted DNA using polymerase chain reaction and the gene products were partially sequenced. The gross and histologic lesions and PCR 18S rDNA gene detection were consistent with that of Histoplasma capsulatum var. duboisii as well as Blastomyces dermatitidis. However, the multiple sequence alignments of the nucleotides showed three mutations that confirmed H. capsulatum. Therefore, there is need for closer examination and monitoring of wild life for mycotic zoonoses.

Keywords

H. duboisii Disseminated Histoplasmosis Green monkey Diagnosis Sequencing Nigeria 

Notes

Acknowledgements

The authors sincerely appreciate management of the University of Ibadan Zoological Garden for providing access to the research animal.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

References

  1. Adekunle OO, Sudhakaran P, Timeyen E (1978) African histoplasmosis of the jejunum: report of a case. J Trop Med Hyg 81:88–90Google Scholar
  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410CrossRefGoogle Scholar
  3. Bialek R, Ibricevic A, Fothergill A, Begerow D (2000) Small-subunit ribosomal DNA sequence shows Paracoccidioides brasiliensis closely related to Blastomyces dermatitidis. J Clin Microbiol 38:3190–3193Google Scholar
  4. Bialek R, Fischer J, Feucht A, Najvar LK, Dietz K, Knobloch J, Graybill JR (2001) Diagnosis and monitoring of murine histoplasmosis by a nested PCR assay. J Clin Microbiol 39:1506–1509CrossRefGoogle Scholar
  5. Bialek R, Cirera AC, Herrmann T, Aepinus C, Shearn-Bochsler VI, Legendre AM (2003) Nested PCR assays for detection of Blastomyces dermatitidis DNA in paraffin-embedded canine tissue. J Clin Microbiol 41(1):205–208CrossRefGoogle Scholar
  6. Bracca A, Tosello ME, Girardini JE, Amigot SL, Gomez C, Serra E (2003) Molecular detection of Histoplasma capsulatum var. capsulatum in human clinical samples. J Clin Microbiol 41:1753–1755CrossRefGoogle Scholar
  7. De Vroey C (1972) Epidemiology of African histoplasmosis. Ann Soc Belg Med Trop 52(4/5):407–420Google Scholar
  8. Fisher KL, Deepe GS Jr, Woods JP (1999) Histoplasma capsulatum strain variation in both H antigen production and beta-glucosidase activity and overexpression of HAG1 from a telomeric linear plasmid. Infect Immun 67:3312–3316Google Scholar
  9. Guedes HL, Guimarães AJ, Muniz Mde M, Pizzini CV, Hamilton AJ, Peralta JM, Deepe GS Jr, Zancopé-Oliveira RM (2003) PCR assay for identification of histoplasma capsulatum based on the nucleotide sequence of the M antigen. J Clin Microbiol 41(2):535–539CrossRefGoogle Scholar
  10. Gugnani HC, Muotoe-Okafor FA, Kaufman L, Dupont B (1994) A natural focus of Histoplasma capsulatum var. duboisii in a bat cave. Mycopathologia 127:151–157CrossRefGoogle Scholar
  11. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  12. Jiang B, Bartlett MS, Allen SD, Smith JW, Wheat LJ, Connolly PA, Lee CH (2000) Typing Histoplasma capsulatum isolates based on nucleotide sequence variation in the internal transcribed spacer regions of rRNA genes. J Clin Microbiol 38:241–245Google Scholar
  13. Kasuga T, Taylor JW, White TJ (1999) Phylogenetic relationships of varieties and geopraphical groups of the human pathogenic fungus Histoplasma capsulatum Darling. J Clin Microbiol 37:653–633Google Scholar
  14. Kauffman CA (2007) Histoplasmosis: a clinical and laboratory update. Clin Microbiol Rev 20:115–132CrossRefGoogle Scholar
  15. Kauffman CA (2009) Histoplasmosis. Clin Chest Med 30(2):217–225CrossRefGoogle Scholar
  16. Keath EJ, Sptzer ED, Painter AA, Travis SJ, Kobayasi GS, Medoff G (1989) DNA probe for the identification of Histoplsma capsulatum. J Clin Microbiol 27:1409–1412Google Scholar
  17. Keath EJ, Kobayashi GS, Medoff G (1992) Typing of Histoplsma capsulatum by restriction fragment length polymorphism in a nuclear gene. J Clin Microbiol 30:2104–2107Google Scholar
  18. Kwon-Chung KJ, Bennett JE (1992) Histoplasmosis. In: Kwon-Chung B (ed) Medical mycology. Lea and Febiger, Philadelphia, pp 464–513Google Scholar
  19. Losnak DO, Rocha FR, Almeida BS, Batista KZS, Althoff SL, Haupt J, Ruiz LS, Anversa L, Lucheis SB, Paiz LM, Donalisio MR, Richini Pereira VB (2018) Molecular detection of fungi of public health importance in wild animals from Southern Brazil. Mycoses 61(7):455–463CrossRefGoogle Scholar
  20. Loulergue P, Bastides F, Baudouin V, Chandenier J, Mariani-Kurkdjian P, Dupont B, Viard JP, Dromer F, Lortholary O (2007) Literature review and case histories of Histoplasma capsulatum var. duboisii infections in HIV-infected patients. Emerg Infect Dis 13(11):1647–1652CrossRefGoogle Scholar
  21. Maubon D, Simon S, Aznar C (2007) Histoplasmosis diagnosis using a polymerase chain reaction method. Application on human samples in French Guiana, South America. Diagn Microbiol Infect Dis 58:441–444CrossRefGoogle Scholar
  22. Muniz MM, Pizzini CV, Peralta JM, Reiss E, Zancopé-Oliveira RM (2001) Genetic diversity of Histoplasma capsulatum strains isolated from soil, animals and specimens in Rio de Janerio State, Brazil by a PCR-based random amplified polymorphic DNA assay. J Clin Microbiol 39(12):4487–4494CrossRefGoogle Scholar
  23. Reyes-Montes MR, Bobadilla-Del Valle M, Martínez-Rivera MA, Rodríguez-Arellanes G, Maravilla E, Sifuentes-Osornio J, Taylor ML (1999) Relatedness analyses of Histoplasma capsulatum isolates from Mexico patients with AID-associated histoplasmosis by using histoplasmin electrophroretic profilrs and randomly amplified polumorphic DNA pattern. J Clin Microbiol 37:1404Google Scholar
  24. Rickerts V, Bialek R, Tintelnot K, Jacobi V, Just-Nubling G (2002) Rapid PCR-based diagnosis of disseminated histoplasmosis in an AIDS patient. Eur J Clin Microbiol Infect Dis 21:821–823CrossRefGoogle Scholar
  25. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425Google Scholar
  26. Sandhu GS, Kline BC, Stockman L, Roberts GD (1995) Molecular probes for diagnosis of fungal infections. J Clin Microbiol 33(11):2913–2919Google Scholar
  27. Spitzer ED, Lasker BA, Travis SJ, Kobayashi GS, Medoff G (1989) Use of mitochondrial and ribosomal DNA polymorphisms to classify clinical and soil isolates of Histoplasma capsulatum. Infect Immun 57(5):1409–1412Google Scholar
  28. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739CrossRefGoogle Scholar
  29. Thompson GR III, LaValle CE III, Everett ED (2004) Unusual manifestations of histoplasmosis. Diagn Microbiol Infect Dis 50:33–41CrossRefGoogle Scholar
  30. Thompson JD, Higgins DG, Gibson TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680CrossRefGoogle Scholar
  31. Woods JP (2002) Histoplasma capsulatum molecular genetics, pathogenesis and responsiveness to its environment. Fungal Genet Biol 35(2):81–97CrossRefGoogle Scholar
  32. Woods JP (2003) Knocking on the right door and making a comfortable home; Histoplasma capsulatum intracellular pathogenesis. Curr Opin Microbiol 6(4):327–331CrossRefGoogle Scholar
  33. Zancope-Oliveira RM, Tavares PMS, Muniz MM (2005) Genetic diversity of Histoplasma capsulatum strains in Brazil. FEMS Immunol Med Microbiol 45:443–449CrossRefGoogle Scholar

Copyright information

© Springer-Verlag London Ltd., part of Springer Nature 2018

Authors and Affiliations

  • O. O. Alaka
    • 1
  • O. A. Fagbohun
    • 2
  • T. A. Jarikre
    • 1
  • V. O. Oyebanji
    • 1
  • R. D. Adesina
    • 2
  • W. U. Anike
    • 1
  • B. C. Okpe
    • 2
  • R. E. Antia
    • 1
  • Benjamin O. Emikpe
    • 1
    Email author
  • S. O. Akpavie
    • 1
  1. 1.Department of Veterinary Pathology, Faculty of Veterinary MedicineUniversity of IbadanIbadanNigeria
  2. 2.Department of Veterinary Microbiology, Faculty of Veterinary MedicineUniversity of IbadanIbadanNigeria

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