1887

Abstract

Purpose. The aim of this study was to assess the biotope of the Cryptococcus neoformans/Cryptococcus gattii species complex from Ivory Coast, and clarify the possible epidemiological relationship between environmental and clinical strains.

Methodology. Samples from Eucalyptus camaldulensis (n=136), Mangifera indica (n=13) and pigeon droppings (n=518) were collected from different sites close to the living environment of Ivorian HIV patients with cryptococcosis (n=10, 50 clinical strains). Clinical and environmental strains were characterized by molecular serotyping and genotyping [RFLP analysis of the URA5 gene, (GACA)4, (GTG)5 and M13 PCR fingerprinting] and compared.

Results/Key findings. Environmental strains were recovered only from the pigeon droppings. In vitro susceptibility profiles showed that all strains were susceptible to fluconazole, flucytosine and amphotericin B. All environmental strains consisted of C. neoformans (A, AFLP1/VNI), whereas clinical strains included C. neoformans (A, AFLP1/VNI), C. neoformans x Cryptococcus deneoformans hybrids (AD, AFLP3/VNIII) and Cryptococcus deuterogattii (B, AFLP6/VGII). Two patients were co-infected with both C. neoformans and C. neoformans x C. deneoformans hybrids. We noticed a low genetic diversity among the environmental samples compared to the high diversity of the clinical samples. Some clinical strains were genetically more similar to environmental strains than to other clinical strains, including those from the same patient.

Conclusion. These results provide new information on the ecology and epidemiology of the C. neoformans/C. gattii species complex in Ivory Coast.

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2017-12-07
2019-10-14
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References

  1. Bicanic T, Meintjes G, Rebe K, Williams A, Loyse A et al. Immune reconstitution inflammatory syndrome in HIV-associated cryptococcal meningitis: a prospective study. J Acquir Immune Defic Syndr 2009; 51: 130– 134 [CrossRef] [PubMed]
    [Google Scholar]
  2. Rajasingham R, Smith RM, Park BJ, Jarvis JN, Govender NP et al. Global burden of disease of HIV-associated cryptococcal meningitis: an updated analysis. Lancet Infect Dis 2017; 17: 873– 881 [CrossRef] [PubMed]
    [Google Scholar]
  3. Hagen F, Khayhan K, Theelen B, Kolecka A, Polacheck I. Recognition of seven species in the Cryptococcus gattii/Cryptococcus neoformans species complex.. Fungal Genet Biol 2015; 78: 16– 48 [Crossref]
    [Google Scholar]
  4. Chen SC, Slavin MA, Heath CH, Playford EG, Byth K et al. Clinical manifestations of Cryptococcus gattii infection: determinants of neurological sequelae and death. Clin Infect Dis 2012; 55: 789– 798 [CrossRef] [PubMed]
    [Google Scholar]
  5. Chen SC, Meyer W, Sorrell TC. Cryptococcus gattii infections. Clin Microbiol Rev 2014; 27: 980– 1024 [CrossRef] [PubMed]
    [Google Scholar]
  6. Chowdhary A, Randhawa HS, Sundar G, Kathuria S, Prakash A et al. In vitro antifungal susceptibility profiles and genotypes of 308 clinical and environmental isolates of Cryptococcus neoformans var. grubii and Cryptococcus gattii serotype B from north-western India. J Med Microbiol 2011; 60: 961– 967 [CrossRef] [PubMed]
    [Google Scholar]
  7. Diaz MR, Boekhout T, Kiesling T, Fell JW. Comparative analysis of the intergenic spacer regions and population structure of the species complex of the pathogenic yeast Cryptococcus neoformans. FEMS Yeast Res 2005; 5: 1129– 1140 [CrossRef] [PubMed]
    [Google Scholar]
  8. Hagen F, Lumbsch HT, Arsic Arsenijevic V, Badali H, Bertout S et al. Importance of resolving fungal nomenclature: the case of multiple pathogenic species in the Cryptococcus genus. mSphere 2017; 2: e00238-17 [CrossRef] [PubMed]
    [Google Scholar]
  9. Kwon-Chung KJ, Wickes BL, Booth JL, Vishniac HS, Bennett JE. Urease inhibition by EDTA in the two varieties of Cryptococcus neoformans. Infect Immun 1987; 55: 1751– 1754 [PubMed]
    [Google Scholar]
  10. Hagen F, Huijsmans A, Klaassen CH, Boekhout T, Meis JF. MALDI-TOF based identification of the pathogenic yeast species C. neoformans and C. gattii. Mycoses 2011; 54: 78 [Crossref]
    [Google Scholar]
  11. Cogliati M. Global molecular epidemiology of Cryptococcus neoformans and Cryptococcus gattii: an atlas of the molecular types. Scientifica 2013; 2013: 1– 23 [CrossRef] [PubMed]
    [Google Scholar]
  12. Espinel-Ingroff A, Aller AI, Canton E, Castañón-Olivares LR, Chowdhary A et al. Cryptococcus neoformans-Cryptococcus gattii species complex: an international study of wild-type susceptibility endpoint distributions and epidemiological cutoff values for fluconazole, itraconazole, posaconazole, and voriconazole. Antimicrob Agents Chemother 2012; 56: 5898– 5906 [CrossRef] [PubMed]
    [Google Scholar]
  13. Espinel-Ingroff A, Chowdhary A, Cuenca-Estrella M, Fothergill A, Fuller J et al. Cryptococcus neoformans-Cryptococcus gattii species complex: an international study of wild-type susceptibility endpoint distributions and epidemiological cutoff values for amphotericin B and flucytosine. Antimicrob Agents Chemother 2012; 56: 3107– 3113 [CrossRef] [PubMed]
    [Google Scholar]
  14. Okubo Y, Wakayama M, Ohno H, Yamamoto S, Tochigi N et al. Histopathological study of murine pulmonary cryptococcosis induced by Cryptococcus gattii and Cryptococcus neoformans. Jpn J Infect Dis 2013; 66: 216– 221 [CrossRef] [PubMed]
    [Google Scholar]
  15. Ngamskulrungroj P, Chang Y, Roh J, Kwon-Chung KJ. Differences in nitrogen metabolism between Cryptococcus neoformans and C. gattii, the two etiologic agents of cryptococcosis. PLoS One 2012; 7: e34258 [CrossRef] [PubMed]
    [Google Scholar]
  16. Giles SS, Dagenais TR, Botts MR, Keller NP, Hull CM. Elucidating the pathogenesis of spores from the human fungal pathogen Cryptococcus neoformans. Infect Immun 2009; 77: 3491– 3500 [CrossRef] [PubMed]
    [Google Scholar]
  17. Velagapudi R, Hsueh YP, Geunes-Boyer S, Wright JR, Heitman J. Spores as infectious propagules of Cryptococcus neoformans. Infect Immun 2009; 77: 4345– 4355 [CrossRef] [PubMed]
    [Google Scholar]
  18. Kangogo M, Bader O, Boga H, Wanyoike W, Folba C et al. Molecular types of Cryptococcus gattii/Cryptococcus neoformans species complex from clinical and environmental sources in Nairobi, Kenya. Mycoses 2015; 58: 665– 670 [CrossRef] [PubMed]
    [Google Scholar]
  19. Litvintseva AP, Kestenbaum L, Vilgalys R, Mitchell TG. Comparative analysis of environmental and clinical populations of Cryptococcus neoformans. J Clin Microbiol 2005; 43: 556– 564 [CrossRef] [PubMed]
    [Google Scholar]
  20. Spina-Tensini T, Muro MD, Queiroz-Telles F, Strozzi I, Moraes ST et al. Geographic distribution of patients affected by Cryptococcus neoformans/Cryptococcus gattii species complexes meningitis, pigeon and tree populations in Southern Brazil. Mycoses 2017; 60: 51– 58 [CrossRef] [PubMed]
    [Google Scholar]
  21. Illnait-Zaragozi MT, Martínez-Machín GF, Fernández-Andreu CM, Boekhout T, Meis JF et al. Microsatellite typing of clinical and environmental Cryptococcus neoformans var. grubii isolates from Cuba shows multiple genetic lineages. PLoS One 2010; 5: e9124 [CrossRef] [PubMed]
    [Google Scholar]
  22. Bertout S, Drakulovski P, Kouanfack C, Krasteva D, Ngouana T et al. Genotyping and antifungal susceptibility testing of Cryptococcus neoformans isolates from Cameroonian HIV-positive adult patients. Clin Microbiol Infect 2013; 19: 763– 769 [CrossRef] [PubMed]
    [Google Scholar]
  23. Klein KR, Hall L, Deml SM, Rysavy JM, Wohlfiel SL et al. Identification of Cryptococcus gattii by use of l-canavanine glycine bromothymol blue medium and DNA sequencing. J Clin Microbiol 2009; 47: 3669– 3672 [CrossRef] [PubMed]
    [Google Scholar]
  24. Clinical and Laboratory Standards Institute Reference Methods for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi, Approved Standard, 2nd ed. Wayne, PA: Clinical Laboratory Standards Institute; 2008
    [Google Scholar]
  25. Pfaller MA, Messer SA, Boyken L, Rice C, Tendolkar S et al. Global trends in the antifungal susceptibility of Cryptococcus neoformans (1990 to 2004). J Clin Microbiol 2005; 43: 2163– 2167 [CrossRef] [PubMed]
    [Google Scholar]
  26. Kassi FK, Drakulovski P, Bellet V, Krasteva D, Gatchitch F et al. Molecular epidemiology reveals genetic diversity among 363 isolates of the Cryptococcus neoformans and Cryptococcus gattii species complex in 61 Ivorian HIV-positive patients. Mycoses 2016; 59: 811– 817 [CrossRef] [PubMed]
    [Google Scholar]
  27. Ito-Kuwa S, Nakamura K, Aoki S, Vidotto V. Serotype identification of Cryptococcus neoformans by multiplex PCR. Mycoses 2007; 50: 277– 281 [CrossRef] [PubMed]
    [Google Scholar]
  28. Kassi FK, Bellet V, Doumbia A, Krasteva D, Drakulovski P et al. First case of mixed infection with Cryptococcus deuterogattii and Cryptococcus neoformans VNI in an Ivorian HIV-positive patient. JMM Case Rep 2016; 3: e005037 [CrossRef] [PubMed]
    [Google Scholar]
  29. Meyer W, Marszewska K, Amirmostofian M, Igreja RP, Hardtke C et al. Molecular typing of global isolates of Cryptococcus neoformans var. neoformans by polymerase chain reaction fingerprinting and randomly amplified polymorphic DNA – a pilot study to standardize techniques on which to base a detailed epidemiological survey. Electrophoresis 1999; 20: 1790– 1799 [CrossRef] [PubMed]
    [Google Scholar]
  30. Trilles L, Fernández-Torres B, Lazéra MS, Wanke B, Guarro J. In vitro antifungal susceptibility of Cryptococcus gattii. J Clin Microbiol 2004; 42: 4815– 4817 [CrossRef] [PubMed]
    [Google Scholar]
  31. Gutch RS, Nawange SR, Singh SM, Yadu R, Tiwari A et al. Antifungal susceptibility of clinical and environmental Cryptococcus neoformans and Cryptococcus gattii isolates in Jabalpur, a city of Madhya Pradesh in Central India. Braz J Microbiol 2015; 46: 1125– 1133 [CrossRef] [PubMed]
    [Google Scholar]
  32. Matos CS, de Souza Andrade A, Oliveira NS, Barros TF. Microbiological characteristics of clinical isolates of Cryptococcus spp. in Bahia, Brazil: molecular types and antifungal susceptibilities. Eur J Clin Microbiol Infect Dis 2012; 31: 1647– 1652 [CrossRef] [PubMed]
    [Google Scholar]
  33. Chen Y, Litvintseva AP, Frazzitta AE, Haverkamp MR, Wang L et al. Comparative analyses of clinical and environmental populations of Cryptococcus neoformans in Botswana. Mol Ecol 2015; 24: 3559– 3571 [CrossRef] [PubMed]
    [Google Scholar]
  34. Bejar V, Tello M, García R, Guevara JM, Gonzales S et al. Molecular characterization and antifungal susceptibility of Cryptococcus neoformans strains collected from a single institution in Lima, Peru. Rev Iberoam Micol 2015; 32: 88– 92 [CrossRef] [PubMed]
    [Google Scholar]
  35. Hagen F, Hare Jensen R, Meis JF, Arendrup MC. Molecular epidemiology and in vitro antifungal susceptibility testing of 108 clinical Cryptococcus neoformans sensu lato and Cryptococcus gattii sensu lato isolates from Denmark. Mycoses 2016; 59: 576– 584 [CrossRef] [PubMed]
    [Google Scholar]
  36. Arsic Arsenijevic V, Pekmezovic MG, Meis JF, Hagen F. Molecular epidemiology and antifungal susceptibility of Serbian Cryptococcus neoformans isolates. Mycoses 2014; 57: 380– 387 [CrossRef] [PubMed]
    [Google Scholar]
  37. Viviani MA, Cogliati M, Esposto MC, Lemmer K, Tintelnot K et al. Molecular analysis of 311 Cryptococcus neoformans isolates from a 30-month ECMM survey of cryptococcosis in Europe. FEMS Yeast Res 2006; 6: 614– 619 [CrossRef] [PubMed]
    [Google Scholar]
  38. Gago S, Serrano C, Alastruey-Izquierdo A, Cuesta I, Martín-Mazuelos E et al. Molecular identification, antifungal resistance and virulence of Cryptococcus neoformans and Cryptococcus deneoformans isolated in Seville, Spain. Mycoses 2017; 60: 40– 50 [CrossRef] [PubMed]
    [Google Scholar]
  39. Cogliati M, Puccianti E, Montagna MT, de Donno A, Susever S et al. Fundamental niche prediction of the pathogenic yeasts Cryptococcus neoformans and Cryptococcus gattii in Europe. Environ Microbiol 2017; 19: 4318– 4325 [CrossRef] [PubMed]
    [Google Scholar]
  40. Desnos-Ollivier M, Patel S, Spaulding AR, Charlier C, Garcia-Hermoso D et al. Mixed infections and in vivo evolution in the human fungal pathogen Cryptococcus neoformans. MBio 2010; 1: e00091-10 [CrossRef] [PubMed]
    [Google Scholar]
  41. Herkert P, Hagen F, Pinheiro R, Muro M, Meis J et al. Ecoepidemiology of Cryptococcus gattii in developing countries. J Fungi 2017; 3: 62 [CrossRef]
    [Google Scholar]
  42. Mahmoud YA. First environmental isolation of Cryptococcus neoformans var. neoformans and var. gatti from the Gharbia Governorate, Egypt. Mycopathologia 1999; 148: 83– 86 [CrossRef] [PubMed]
    [Google Scholar]
  43. Mseddi F, Sellami A, Jarboui MA, Sellami H, Makni F et al. First environmental isolations of Cryptococcus neoformans and Cryptococcus gattii in Tunisia and review of published studies on environmental isolations in Africa. Mycopathologia 2011; 171: 355– 360 [CrossRef] [PubMed]
    [Google Scholar]
  44. Nnadi NE, Enweani IB, Cogliati M, Ayanbimpe GM, Okolo MO et al. Molecular characterization of environmental Cryptococcus neoformans VNII isolates in Jos, Plateau State, Nigeria. J Mycol Med 2016; 26: 306– 311 [CrossRef] [PubMed]
    [Google Scholar]
  45. Ellabib MS, Aboshkiwa MA, Husien WM, D'Amicis R, Cogliati M. Isolation, identification and molecular typing of Cryptococcus neoformans from pigeon droppings and other environmental sources in Tripoli, Libya. Mycopathologia 2016; 181: 603– 608 [CrossRef] [PubMed]
    [Google Scholar]
  46. Park SH, Choi SC, Lee KW, Kim MN, Hwang SM. Genotypes of clinical and environmental isolates of Cryptococcus neoformans and Cryptococcus gattii in Korea. Mycobiology 2015; 43: 360– 365 [CrossRef] [PubMed]
    [Google Scholar]
  47. Kammalac Ngouana T, Dongtsa J, Kouanfack C, Tonfack C, Fomena S et al. Cryptoccocal meningitis in Yaoundé (Cameroon) HIV infected patients: diagnosis, frequency and Cryptococcus neoformans isolates susceptibility study to fluconazole. J Mycol Med 2015; 25: 11– 16 [CrossRef] [PubMed]
    [Google Scholar]
  48. Yamamoto Y, Kohno S, Koga H, Kakeya H, Tomono K et al. Random amplified polymorphic DNA analysis of clinically and environmentally isolated Cryptococcus neoformans in Nagasaki. J Clin Microbiol 1995; 33: 3328– 3332 [PubMed]
    [Google Scholar]
  49. Escandón P, Sánchez A, Martínez M, Meyer W, Castañeda E. Molecular epidemiology of clinical and environmental isolates of the Cryptococcus neoformans species complex reveals a high genetic diversity and the presence of the molecular type VGII mating type a in Colombia. FEMS Yeast Res 2006; 6: 625– 635 [CrossRef] [PubMed]
    [Google Scholar]
  50. Baker LG, Specht CA, Donlin MJ, Lodge JK. Chitosan, the deacetylated form of chitin, is necessary for cell wall integrity in Cryptococcus neoformans. Eukaryot Cell 2007; 6: 855– 867 [CrossRef] [PubMed]
    [Google Scholar]
  51. Movahed E, Munusamy K, Tan GM, Looi CY, Tay ST et al. Genome-wide transcription study of Cryptococcus neoformans H99 clinical strain versus environmental strains. PLoS One 2015; 10: e0137457 [CrossRef] [PubMed]
    [Google Scholar]
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