Diversity, Virulence Factors, and Antifungal Susceptibility Patterns of Pathogenic and Opportunistic Yeast Species in Rock Pigeon (Columba livia) Fecal Droppings in Western Saudi Arabia

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Polish Journal of Microbiology

Polish Society of Microbiologists

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VOLUME 68 , ISSUE 4 (Jan 2019) > List of articles

Diversity, Virulence Factors, and Antifungal Susceptibility Patterns of Pathogenic and Opportunistic Yeast Species in Rock Pigeon (Columba livia) Fecal Droppings in Western Saudi Arabia

HUSSEIN H. ABULREESH * / SAMEER R. ORGANJI / KHALED ELBANNA / GAMAL E.H. OSMAN / MESHAL H.K. ALMALKI / AHMED Y. ABDEL-MALEK / ABDULLAH A.K. GHYATHUDDIN / IQBAL AHMAD

Keywords : Cryptococcus, pigeon, fecal droppings, antifungal susceptibility, virulence genes, yeast

Citation Information : Polish Journal of Microbiology. Volume 68, Issue 4, Pages 493-504, DOI: https://doi.org/10.33073/pjm-2019-049

License : (CC-BY-NC-ND 4.0)

Published Online: 05-December-2019

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  1. Abbass MS, Yassein SN, Khalaf JM. Isolation and identification of some important mycological isolates from droppings of birds in Baghdad. J Entomol Zool Stud. 2017;5:671–673.
  2. Abulreesh H. Faecal shedding of antibiotic resistant Escherichia coli serogroups in pigeons with special reference to E. coli O157. Annu Res Rev Biol. 2014 Jan 10;4(13):2184–2191. https://doi.org/10.9734/ARRB/2014/9501
    [CROSSREF]
  3. Abulreesh HH, Goulder R, Scott GW. Wild birds and human patho gens in the context of ringing and migration. Ring Migr. 2007 Jan; 23(4):193–200. https://doi.org/10.1080/03078698.2007.9674363
    [CROSSREF]
  4. Abulreesh HH, Organji SR, Elbanna K, Osman GEH, Almalki MHK, Abdel-Mallek AY. First report of environmental isolation of Cryptococcus neoformans and other fungi from pigeon droppings in Makkah, Saudi Arabia and in vitro susceptibility testing. Asian Pac J Trop Dis. 2015 Aug;5(8):622–626. https://doi.org/10.1016/S2222-1808(15)60901-X
    [CROSSREF]
  5. Alspaugh JA. Virulence mechanisms and Cryptococcus neoformans pathogenesis. Fungal Genet Biol. 2015 May;78:55–58. https://doi.org/10.1016/j.fgb.2014.09.004
    [PUBMED] [CROSSREF]
  6. Al-Tawfiq JA, Ghandour J. Cryptococcus neoformans abscess and osteomyelitis in an immunocompetent patient with tuberculous lym phadenitis. Infection. 2007 Oct;35(5):377–382. https://doi.org/10.1007/s15010-007-6109-9
    [PUBMED] [CROSSREF]
  7. Boral H, Metin B, Döğen A, Seyedmousavi S, Ilkit M. Overview of selected virulence attributes in Aspergillus fumigatus, Candida albicans, Cryptococcus neoformans, Trichophyton rubrum, and Exophiala dermatitidis. Fungal Genet Biol. 2018 Feb;111:92–107. https://doi.org/10.1016/j.fgb.2017.10.008
    [PUBMED] [CROSSREF]
  8. Burnik C, Altintaş ND, Özkaya G, Serter T, Selçuk ZT, Firat P, Arikan S, Cuenca-Estrella M, Topeli A. Acute respiratory distress syndrome due to Cryptococcus albidus pneumonia: case report and review of the literature. Med Mycol. 2007 Jan;45(5):469–473. https://doi.org/10.1080/13693780701386015
    [PUBMED] [CROSSREF]
  9. Cafarchia C, Romito D, Coccioli C, Camarda A, Otranto D. Phospholipase activity of yeasts from wild birds and possible implications for human disease. Med Mycol. 2008 Jan;46(5):429–434. https://doi.org/10.1080/13693780701885636
    [PUBMED] [CROSSREF]
  10. Canónico-González Y, Adame-Rodríguez JM, Mercado-Hernández R, Aréchiga-Carvajal ET. Cryptococcus spp. isolation from excreta of pigeons (Columba livia) in and around Monterrey, Mexico. SpringerPlus. 2013 Dec;2(1):632. https://doi.org/10.1186/2193-1801-2-632
    [PUBMED] [CROSSREF]
  11. Canteros CE, Rodero L, Rivas MC, Davel G. A rapid urease test for presumptive identification of Cryptococcus neoformans. Mycopatho logia. 1996 Oct;136(1):21–23. https://doi.org/10.1007/BF00436656
    [CROSSREF]
  12. Cebeci Güler N, Tosun İ, Aydin F. The identification of Meyerozyma guilliermondii from blood cultures and surveillance samples in a university hospital in Northeast Turkey: A ten-year survey. J Mycol Med. 2017 Dec;27(4):506–513. https://doi.org/10.1016/j.mycmed.2017.07.007
    [CROSSREF]
  13. Chae HS, Jang GE, Kim NH, Son HR, Lee JH, Kim SH, Park GN, Jo HJ, Kim JT, Chang KS. Classification of Cryptococcus neoformans and yeast-like fungus isolates from pigeon droppings by colony phenotyping and ITS genotyping and their seasonal variations in Korea. Avian Dis. 2012 Mar;56(1):58–64. https://doi.org/10.1637/9703-030711-Reg.1
    [PUBMED] [CROSSREF]
  14. Chowdhary A, Hiremath SS, Sun S, Kowshik T, Randhawa HS, Xu J. Genetic differentiation, recombination and clonal expansion in environmental populations of Cryptococcus gattii in India. Environ Microbiol. 2011 Jul;13(7):1875–1888. https://doi.org/10.1111/j.1462-2920.2011.02510.x
    [PUBMED] [CROSSREF]
  15. Cleveland KO, Gelfand MS, Rao V. Posaconazole as successful treatment for fungemia due to Cryptococcus albidus in a liver transplant recipient. QJM. 2013 Apr 01;106(4):361–362. https://doi.org/10.1093/qjmed/hcs133
    [PUBMED] [CROSSREF]
  16. CLSI. Method for antifungal susceptibility testing of yeasts. Approved Standard M44-A2. Wayne (PA, USA): Clinical and Laboratory Standards Institute; 2008.
  17. Cogliati M. Global epidemiology of Cryptococcus neoformans and Cryptococcus gattii: An atlas of the molecular types. Scientifica. 2013; Article ID 675213, 23 pages.
  18. Costa AKF, Sidrim JJC, Cordeiro RA, Brilhante RSN, Monteiro AJ, Rocha MFG. Urban pigeons (Columba livia) as a potential source of pathogenic yeasts: a focus on antifungal susceptibility of Cryptococcus strains in Northeast Brazil. Mycopathologia. 2010 Mar;169(3):207–213. https://doi.org/10.1007/s11046-009-9245-1
    [CROSSREF]
  19. Delgado ACN, Taguchi H, Mikami Y, Myiajy M, Villares MCB, Moretti ML. Human cryptococcosis: relationship of environmental and clinical strains of Cryptococcus neoformans var. neoformans from urban and rural areas. Mycopathologia. 2005 Jan;159(1):7–11. https://doi.org/10.1007/s11046-004-9618-4
    [CROSSREF]
  20. Duggal S, Jain H, Tyagi A, Sharma A, Chugh TD. Rhodotorula fungemia: two cases and a brief review. Med Mycol. 2011 Nov;49(8):879–882.
    [PUBMED]
  21. Esher SK, Zaragoza O, Alspaugh JA. Cryptococcal pathogenic mechanisms: a dangerous trip from the environment to the brain. Mem Inst Oswaldo Cruz. 2018;113(7):e180057. https://doi.org/10.1590/0074-02760180057
    [CROSSREF]
  22. Fan Y, Pan W, Wang G, Huang Y, Li Y, Fang W, Tao X. Isolated cutaneous granuloma caused by Candida glabrata: A rare case report and literature review. Mycopathologia. 2018 Apr;183(2):417–421. https://doi.org/10.1007/s11046-017-0228-3
    [PUBMED] [CROSSREF]
  23. Feder V, Kmetzsch L, Staats CC, Vidal-Figueiredo N, Ligabue-Braun R, Carlini CR, Vainstein MH. Cryptococcus gattii urease as a virulence factor and the relevance of enzymatic activity in cryptococcosis pathogenesis. FEBS J. 2015 Apr;282(8):1406–1418. https://doi.org/10.1111/febs.13229
    [PUBMED] [CROSSREF]
  24. Gagliano M, Marchiani C, Bandini G, Bernardi P, Palagano N, Cioni E, Finocchi M, Bellando Randone S, Moggi Pignone A. A rare case of Candida glabrata spondylodiscitis: case report and literature review. Int J Infect Dis. 2018 Mar;68:31–35. https://doi.org/10.1016/j.ijid.2018.01.003
    [PUBMED] [CROSSREF]
  25. Govender NP, Patel J, van Wyk M, Chiller TM, Lockhart SR. Group for Enteric, Respiratory and Meningeal Disease Surveillance in South Africa (GERMS-SA). Trends in antifungal drug susceptibility of Cryptococcus neoformans isolates obtained through population-based surveillance in South Africa in 2002–2003 and 2007– 2008. Antimicrob Agents Chemother. 2011 Jun;55(6):2606–2611. https://doi.org/10.1128/AAC.00048-11
    [PUBMED] [CROSSREF]
  26. Haag-Wackernagel D, Moch H. Health hazards posed by feral pigeons. J Infect. 2004 May;48(4):307–313. https://doi.org/10.1016/j.jinf.2003.11.001
    [PUBMED] [CROSSREF]
  27. Hagen F, Khayhan K, Theelen B, Kolecka A, Polacheck I, Sionov E, Falk R, Parnmen S, Lumbsch HT, Boekhout T. Recognition of seven species in the Cryptococcus gattii/Cryptococcus neoformans species complex. Fungal Genet Biol. 2015 May;78:16–48. https://doi.org/10.1016/j.fgb.2015.02.009
    [PUBMED] [CROSSREF]
  28. Hashemi SJ, Jabbari AG, Bayat M, Rafiei SM. Prevalence of Crypto coccus neoformans in domestic birds referred to veterinary clinics in Tehran. Eur J Exp Biol. 2014;4:482–486.
  29. Hatanaka S, Nakamura I, Fukushima S, Ohkusu K, Matsumoto T. Cather-related bloodstream infection due to Lodderomyces elongisporus. Jpn J Infect Dis. 2016;69(6):520–522. https://doi.org/10.7883/yoken.JJID.2015.307
    [PUBMED] [CROSSREF]
  30. Hof H, Amann V, Tauber C, Paulun A. Peritonitis in a neonate due to Cyberlindnera fabianii, an ascomycetic yeast. Infection. 2017 Dec;45(6):921–924. https://doi.org/10.1007/s15010-017-1062-8
    [PUBMED] [CROSSREF]
  31. Kitazawa T, Ishigaki S, Seo K, Yoshino Y, Ota Y. Catheter-related bloodstream infection due to Rhodotorula mucilaginosa with normal serum (1→3)-β-D-glucan level. J Mycol Med. 2018 Jun; 28(2):393–395. https://doi.org/10.1016/j.mycmed.2018.04.001
    [CROSSREF]
  32. Kontoyiannis DP. Antifungal resistance: an emerging reality and a global challenge. J Infect Dis. 2017 Aug 15;216 suppl_3:S431–S435. https://doi.org/10.1093/infdis/jix179
    [PUBMED] [CROSSREF]
  33. Koutserimpas C, Samonis G, Velivassakis E, Iliopoulou-Kosmadaki S, Kontakis G, Kofteridis DP. Candida glabrata prosthetic joint infection, successfully treated with anidulafungin: A case report and review of the literature. Mycoses. 2018 Apr;61(4):266–269. ttps://doi.org/10.1111/myc.12736
    [PUBMED] [CROSSREF]
  34. Liaw S-J, Wu H-C, Hsueh P-R. Microbiological characteristics of clinical isolates of Cryptococcus neoformans in Taiwan: serotypes, mating types, molecular types, virulence factors, and antifungal susceptibility. Clin Microbiol Infect. 2010 Jun;16(6):696–703. https://doi.org/10.1111/j.1469-0691.2009.02930.x
    [PUBMED] [CROSSREF]
  35. Lotfalikhani A, Khosravi Y, Sabet NS, Na SL, Ng KP, Tay ST. Genetic diversity, antifungal susceptibility and enzymatic characterization of Malaysian clinical isolates of Candida glabrata. Trop Biomed. 2018;35:1123–1130.
  36. Magalhães Pinto L, de Assis Bezerra Neto F, Araújo Paulo de Medeiros M, Zuza Alves DL, Maranhão Chaves G. Candida species isolated from pigeon (Columbia livia) droppings may express virulence factors and resistance to azoles. Vet Microbiol. 2019 Aug; 235:43–52. https://doi.org/10.1016/j.vetmic.2019.05.022
    [PUBMED] [CROSSREF]
  37. Mahmoud YAG. First environmental isolation of Cryptococcus neoformans var. neoformans and var. gatti from the Gharbia Governorate, Egypt. Mycopathologia. 1999;148(2):83–86. https://doi.org/10.1023/A:1007166818993
    [CROSSREF]
  38. Marenzoni ML, Morganti G, Moretta I, Crotti S, Agnetti F, Moretti A, Pitzurra L, Casagrande Proietti P, Sechi P, Cenci-Goga B, et al. Microbiological and parasitological survey of zoonotic agents in apparently healthy feral pigeons. Pol J Vet Sci. 2016 Jun 1;19(2):309–315. https://doi.org/10.1515/pjvs-2016-0038
    [CROSSREF]
  39. Mattsson R, Haemig PD, Olsen B. Feral pigeons as carriers of Cryptococcus laurentii, Cryptococcus uniguttulatus and Debaryomyces hansenii. Med Mycol. 1999 Oct;37(5):367–369. https://doi.org/10.1046/j.1365-280X.1999.00241.x
    [PUBMED] [CROSSREF]
  40. Miceli MH, Díaz JA, Lee SA. Emerging opportunistic yeast infections. Lancet Infect Dis. 2011 Feb;11(2):142–151. https://doi.org/10.1016/S1473-3099(10)70218-8
    [PUBMED] [CROSSREF]
  41. Milanezi ACM, Witusk JPD, VAN DER Sand ST. Antifungal susceptibility of yeasts isolated from anthropogenic watershed. An Acad Bras Cienc. 2019;91(1):e20170369.
  42. Miranda-Cadena K, Marcos-Arias C, Mateo E, Aguirre JM, Quindós G, Eraso E. Prevalence and antifungal susceptibility profiles of Candida glabrata, Candida parapsilosis and their close-related species in oral candidiasis. Arch Oral Biol. 2018 Nov;95:100–107. https://doi.org/10.1016/j.archoralbio.2018.07.017
    [PUBMED] [CROSSREF]
  43. Mseddi F, Sellami A, Jarboui MA, Sellami H, Makni F, Ayadi A. First environmental isolations of Cryptococcus neoformans and Crypto coccus gattii in Tunisia and review of published studies on environmental isolation in Africa. Mycopathologia. 2011 May; 171(5):355–360. https://doi.org/10.1007/s11046-010-9381-7
    [PUBMED] [CROSSREF]
  44. Nenoff P, Krüger C, Neumeister C, Schwantes U, Koch D. In vitro susceptibility testing of yeasts to nystatin – low minimum inhibitory concentrations suggest no indication of in vitro resistance of Candida albicans, Candida species or non-Candida yeast species to nystatin. Clin Med Invest. 2016;1(3):71–76. https://doi.org/10.15761/CMI.1000116
    [CROSSREF]
  45. Pincus DH, Orenga S, Chatellier S. Yeast identification – past, present, and future methods. Med Mycol. 2007 Jan;45(2):97–121. https://doi.org/10.1080/13693780601059936
    [PUBMED] [CROSSREF]
  46. Popiel KY, Wong P, Lee MJ, Langelier M, Sheppard DC, Vinh DC. Invasive Saccharomyces cerevisiae in a liver transplant patient: case report and review of infection in transplant recipients. Transpl Infect Dis. 2015 Jun;17(3):435–441. https://doi.org/10.1111/tid.12384
    [PUBMED] [CROSSREF]
  47. Rajasingham R, Smith RM, Park BJ, Jarvis JN, Govender NP, Chiller TM, Denning DW, Loyse A, Boulware DR. Global burden of disease of HIV-associated cryptococcal meningitis: an updated analysis. Lancet Infect Dis. 2017 Aug;17(8):873–881. https://doi.org/10.1016/S1473-3099(17)30243-8
    [PUBMED] [CROSSREF]
  48. Razzaq Abed A, Mohammed Hussein I. A comparative study between specific and non-specific antifungal agents to treat the Rhodotorula mucilaginosa athletes foot. Biomed Pharmacol J. 2017 Dec 28;10(4):2153–2160. https://doi.org/10.13005/bpj/1340
    [CROSSREF]
  49. Rosario I, Soro G, Déniz S, Ferrer O, Acosta F, Padilla D, Acosta B. Presence of C. albidus, C. laurentii and C. uniguttulatus in crop and droppings of pigeon lofts (Columba livia). Mycopathologia. 2010 Apr;169(4):315–319. https://doi.org/10.1007/s11046-009-9262-0
    [PUBMED] [CROSSREF]
  50. Rosario Medina I, Román Fuentes L, Batista Arteaga M, Real Valcárcel F, Acosta Arbelo F, Padilla del Castillo D, Déniz Suárez S, Ferrer Quintana O, Vega Gutiérrez B, Silva Sergent F, et al. Pigeons and their droppings as reservoirs of Candida and other zoonotic yeasts. Rev Iberoam Micol. 2017 Oct;34(4):211–214. https://doi.org/10.1016/j.riam.2017.03.001
    [PUBMED] [CROSSREF]
  51. Soltani M, Bayat M, Hashemi SJ, Zia M, Pestechian N. Isolation of Cryptococcus neoformans and other opportunistic fungi from pigeon droppings. J Res Med Sci. 2013 Jan;18(1):56–60.
    [PUBMED]
  52. Souza LKH, Souza Junior AH, Costa CR, Faganello J, Vainstein MH, Chagas ALB, Souza ACM, Silva MRR. Molecular typing and antifungal susceptibility of clinical and environmental Cryptococcus neoformans species complex isolates in Goiania, Brazil. Mycoses. 2010 Jan;53(1):62–67. https://doi.org/10.1111/j.1439-0507.2008.01662.x
    [PUBMED] [CROSSREF]
  53. Srikanta D, Santiago-Tirado FH, Doering TL. Cryptococcus neoformans: historical curiosity to modern pathogen. Yeast. 2014 Feb;31(2):47–60. https://doi.org/10.1002/yea.2997
    [PUBMED] [CROSSREF]
  54. Tangwattanachuleeporn M, Somparn P, Poolpol K, Gross U, Weig M, Bader O. Prevalence and antifungal susceptibility of Cryptococcus neoformans isolated from pigeon excreta in Chon Buri Province, Eastern Thailand. Med Mycol J. 2013;54(3):303–307. https://doi.org/10.3314/mmj.54.303
    [CROSSREF]
  55. Teodoro VLI, Gullo FP, Sardi JCO, Torres EM, Fusco-Almeida AM, Mendes-Giannini MJS. Environmental isolation, biochemical identification, and antifungal drug susceptibility of Cryptococcus species. Rev Soc Bras Med Trop. 2013 Dec;46(6):759–764. https://doi.org/10.1590/0037-8682-0025-2013
    [PUBMED] [CROSSREF]
  56. White TJ, Bruns TD, Lee SB, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR Protocols: A guide to methods and applications. New York (USA): Academic Press; 1990. p. 315–322. http://doi.org/10.1016/B978-0-12-372180-8.50042-1
  57. Wirth F, Goldani LZ. Epidemiology of Rhodotorula: an emerging pathogen. Interdiscip Perspect Infect Dis. 2012;2012:1–7. https://doi.org/10.1155/2012/465717
    [CROSSREF]
  58. Wu Y, Du PC, Li WG, Lu JX. Identification and molecular analysis of pathogenic yeasts in droppings of domestic pigeons in Beijing, China. Mycopathologia. 2012 Sep;174(3):203–214. https://doi.org/10.1007/s11046-012-9536-9
    [PUBMED] [CROSSREF]
  59. Xavier TF, Auxilia A, Kannan M, Freeda Rose A, Senthil Kumar SR. Isolation and identification of Cryptococcus neoformans from pigeon droppings in Tiruchirapalli district of Tamil Nadu, south India. Int J Curr Microbiol Appl Sci. 2013;2:404–409.
  60. Zhu Z, Huang Z, Li Z, Li X, Du C, Tian Y. Multiple brain abscesses caused by infection with Candida glabrata: A case report. Exp Ther Med. 2018 Mar;15(3):2374–2380.
    [PUBMED]

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