Keratitis by Fusarium temperatum, a novel opportunist

BMC Infectious Diseases

Anne D van Diepeningen³  Jacques F Meis¹  Karla Garcia-Carmona⁴  Leticia Vazquez-Maya⁴  G Sybren de Hoog²  Alexandro Bonifaz⁴  Abdullah M S Al-Hatmi⁵ 

[1] Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, the Netherlands;King Abdulaziz University, Jeddah, Saudi Arabia;CBS-KNAW Fungal Biodiversity Centre, Utrecht, 3508 AD, the Netherlands;Hospital General de México, O.D, Mexico City, Mexico;Directorate General of Health Services, Ibri Hospital, Ministry of Health, Muscat, Oman

关键词: Infection;    Molecular phylogenetics;    Maize;    Fusarium temperatum;    Keratitis;   

Others  :  1122088
DOI  :  10.1186/s12879-014-0588-y

 received in 2014-06-01, accepted in 2014-10-24,  发布年份 2014

【 摘 要 】

Background

Fusarium species are among the most common fungi present in the environment and some species have emerged as major opportunistic fungal infection in human. However, in immunocompromised hosts they can be virulent pathogens and can cause death. The pathogenesis of this infection relies on three factors: colonization, tissue damage, and immunosuppression. A novel Fusarium species is reported for the first time from keratitis in an agriculture worker who acquired the infection from plant material of maize. Maize plants are the natural host of this fungus where it causes stalk rot and seeding malformation under temperate and humid climatic conditions. The clinical manifestation, microbiological morphology, physiological features and molecular data are described.

Methods

Diagnosis was established by using polymerase chain reaction of fungal DNA followed by sequencing portions of translation elongation factor 1 alpha (TEF1 α) and beta-tubulin (BT2) genes. Susceptibility profiles of this fungus were evaluated using CLSI broth microdilution method.

Results

The analyses of these two genes sequences support a novel opportunist with the designation Fusarium temperatum. Phylogenetic analyses showed that the reported clinical isolate was nested within the Fusarium fujikuroi species complex. Antifungal susceptibility testing demonstrated that the fungus had low MICs of micafungin (0.031 μg/ml), posaconazole (0.25 μg/ml) and amphotericin B (0.5 μg/ml).

Conclusion

The present case extends the significance of the genus Fusarium as agents of keratitis and underscores the utility of molecular verification of these emerging fungi in the human host.

【 授权许可】

   
2014 Al-Hatmi et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

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【 参考文献 】

• [1]Liesegang TJ, Forster RF: Spectrum of microbial keratitis in South Florida. Am J Ophthalmol 1980, 90:38-47.
• [2]Ibrahim MM, Vanini R, Ibrahim FM, Fioriti LS, Furlan EM, Provinzano LM, De Castro RS, de Faria E, Sousa SJ, Melani Rocha E: Epidemiologic aspects and clinical outcome of fungal keratitis in southeastern Brazil. Eur J Ophthalmol 2009, 19:355-361.
• [3]Galarreta DJ, Tuft SJ, Ramsay A, Dart JK: Fungal keratitis in London: microbiological and clinical evaluation. Cornea 2007, 26:1082-1086.
• [4]Dóczi I, Gyetvai T, Kredics L, Nagy E: Involvement of Fusarium spp. in fungal keratitis. Clin Microbiol Infect 2004, 10:773-776.
• [5]Guarro J, Gene J: Opportunistic fusarial infections in humans. Eur J Clin Microbiol Infect Dis 1995, 14:741-754.
• [6]Bernal MD, Acharya NR, Lietman TM, Strauss EC, McLeod SD, Hwang DG: Outbreak of Fusarium keratitis in soft contact lens wearers in San Francisco. Arch Ophthalmol 2006, 124:1051-1053.
• [7]Chander J, Sharma A: Prevalence of fungal corneal ulcers in northern India. Infection 1994, 22:207-209.
• [8]Polack FM, Kaufman HE, Newmark E: Keratomycosis. Medical and surgical treatment. Arch Ophthalmol 1971, 85:410-416.
• [9]Homa M, Shobana CS, Singh YR, Manikandan P, Selvam KP, Kredics L, Narendran V, Vágvölgyi C, Galgóczy L: Fusarium keratitis in South India: causative agents, their antifungal susceptibilities and a rapid identification method for the Fusarium solani species complex. Mycoses 2013, 56:501-11.
• [10]Kebabc N, van Diepeningen AD, Ener B, Ersal T, Meijer M, Al-Hatmi AMS, Özkocaman V, Ursavaş A, Çetinoğlu ED, Akalın H: Fatal breakthrough infection with Fusarium andiyazi: new multi-resistant aetiological agent cross-reacting with Aspergillus galactomannan enzyme immunoassay. Mycoses 2014, 57:249-255.
• [11]Jain PK, Gupta VK, Misra AK, Gaur R, Bajpai V, Issar S: Current status of Fusarium infection in human and animal. Asian J Anim Veter Adv 2011, 6:201-227.
• [12]Nucci M, Anaissie E: Fusarium infections in immunocompromised patients. Clin Microbiol Rev 2007, 20:695-704.
• [13]Mikami R, Stemmermann GN: Keratomycosis caused by Fusarium oxysporum. Am J Clin Pathol 1958, 29:257-262.
• [14]Gupta AK, Baran R, Summerbell RC: Fusarium infections of the skin. Curr Opin Infect Dis 2000, 13:121-128.
• [15]Nirenberg HI: Untersuchungen uber die morphologische und biologische differenzierung in der Fusarium Sektion Liseola. Mitteilungen aus der Biologischen Bundesanstalt für Land- und Forstwirtschaft (Berlin-Dahlem) 1976, 169:1-117.
• [16]Leslie JF, Summerell BA: The Fusarium Laboratory Manual. Blackwell Publishing Ltd, Ames, Oxford; 2006.
• [17]O’Donnell K, Sutton DA, Rinaldi MG, Sarver BA, Balajee SA, Schroers HJ, Summerbell RC, Robert VA, Crous PW, Zhang N, Aoki T, Jung K, Park J, Lee YH, Kang S, Park B, Geiser DM: Internet-accessible DNA sequence database for identifying fusaria from human and animal infections. J Clin Microbiol 2010, 48:3708-3718.
• [18]Glass NL, Donaldson G: Development of primer sets designed for use with PCR to amplify conserved genes from filamentous ascomycetes. Appl Environm Microbiol 1995, 61:1323-1330.
• [19]O’Donnel K, Cigelnik E: Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol 1997, 7:103-116.
• [20]Reference Method for Broth Dilution Antifungal Susceptibility Testing for Filamentous Fungi; Approved Standard. Document M38-A2. Clinical and Laboratory Standards Institute, Wayne, PA; 2008.
• [21]Srinivasan M: Fungal keratitis. Curr Opin Ophthalmol 2004, 15:321-327.
• [22]Guarro J: Fusariosis, a complex infection caused by a high diversity of fungal species refractory to treatment. Eur J Clin Microbiol Infect Dis 2013, 32:1491-1500.
• [23]Chowdhary A, Singh K: Spectrum of fungal keratitis in North India. Cornea 2005, 24:8-15.
• [24]Punia RS, Kundu R, Chander J, Arya SK, Handa U, Mohan H: Spectrum of fungal keratitis: clinicopathologic study of 44 cases. Int J Opthalmol 2014, 7:114-117.
• [25]Short DP, O’Donnell K, Thrane U, Nielsen KF, Zhang N, Juba JH, Geiser DM: Phylogenetic relationships among members of the fusarium solani species complex in human infections and the descriptions of F. Keratoplasticum sp. nov. and F. petroliphilum stat. nov. Fungal Genet Biol 2013, 53:59-70.
• [26]Knogge W: Fungal infection of plants. The Plant Cell 1996, 8:1711-1722.
• [27]Geiser D, Jimenez-Gasco M, Kang S, Veeraraghavan I, Ward T, Zhang N, Kuldau G, O’Donnell K: FUSARIUM-ID v. 1.0: a DNA sequence database for identifying Fusarium. Eur J Plant Pathol 2004, 110:473-479.
• [28]O’Donnell K, Nirenberg H, Takayuki A, Cigelnik E: A multigene phylogeny of the Gibberella fujikuroi species complex: detection of additional phylogenetically distinct species. Mycoscience 2000, 41:61-78.
• [29]Guarro J, Gene J, Stchigel A: Developments in fungal taxonomy. Clin Microbiol Rev 1999, 12:454-500.
• [30]Smith SN: An overview of ecological and habitat aspects in the genus Fusarium with special emphasis on the soil-borne pathogenic forms. Plant Pathol Bull 2007, 16:97-120.
• [31]Coulumbe RA: Biological action of mycotoxins. J Dairy Sci 1993, 76:880-891.
• [32]Tabatabaee A, Mohajernezhadfard Z, Daneshgar F, Mansouri M: Keratomycosis after incidental spillage of vegetative material into the eye: report of two cases. Oman J Ophthalmol 2013, 6:122-126.
• [33]Mehl HL, Epstein L: Fusarium soloni species complex isolates conspecific with Fusarium solani f. sp. cucurbitae race 2 from naturally infected human and plant tissue and environmental sources are equally virulent on plants, grow at 37°C and are interfertile. Environ Microbiol 2007, 9:2189-2199.
• [34]Zhang N, O’Donnell K, Sutton DA, Nalim FA, Summerbell RC, Padhye AA, Geiser DM: Members of the Fusarium solani species complex that cause infection in both humans and plants are common in the environment. J Clin Microbiol 2006, 44:2186-2190.
• [35]Ortoneda M, Guarro J, Madrid MP, Caracuel Z, Roncero M, Mayayo E, Pietro A: Fusarium oxysporum as a multihost model for the genetic dissection of fungal virulence in plants and mammals. Infect Immun 2004, 72:1760-1766.
• [36]Lew HJ, Chelkowski J, Pronczuk P, Edinger W: Occurrence of the mycotoxin moniliformin in maize (Zea mays L.) ears infected by Fusarium subglutinans. Food Addit Contam 1996, 13:321-324.
• [37]Edwards ET: Studies on the Gibberella fujikuroi var. subglutinans the hitherto undescribed ascigerous stage of Fusarium moniliforme var. subglutinans and its pathogenicity on maize in New South Wales. Dep Agric New South Wales Sci Bull 1935, 49:1-68.
• [38]Marasas WFO, Rheeder JP, Lamprecht SC, Zeller KA, Leslie JF: Fusarium andiyazi sp.nov., a new species from sorghum. Mycologia 2001, 93:1203-1210.
• [39]Britz H, Coutinho TA, Wingfield MJ, Marasas WFO, Gordon TR, Leslie JF: Fusarium subglutinans f. sp. pini represents a distinct mating population in the Giberrella fujikuroi species complex. Appl Environ Microbiol 1999, 65:1198-1201.
• [40]Scauflaire J, Gourgue M, Munaut F: Fusarium temperatum sp. nov. from maize, an emergent species closely related to Fusarium subglutinans. Mycologia 2011, 103:586-597.
• [41]Scauflaire J, Gourgue M, Callebaut A, Munant F: Fusarium temperatum, a mycotoxin-producing pathogen of maize. Eur J Plant Pathol 2012, 133:911-922.
• [42]Pintos V, Aguín C, Chaves P, Ferreiroa-Martínez V, Sainz M, Scauflaire J, Munaut F, Mansilla V: First report of fusarium temperatum causing seedling blight and stalk Rot on maize in Spain. Plant Dis 2013, 97:1252-1252.
• [43]Van Baarlen P, Van Belkum A, Summerbell R, Crous PW, Thomma B: Molecular mechanisms of pathogenicity: how do pathogenic microorganisms develop cross-kingdom host jumps? FEMS Microbiol Rev 2007, 31:239-277.
• [44]De Hoog G, Guarro J, Gene J, Figueras MJ: Atlas of Clinical Fungi. Centraalbureau voor Schimmelcultures, Utrecht, the Netherlands; 2000.
• [45]Vanzzini V, Manzano-Gayosso P, Hernández-Hernández F, Méndez-Tovar LJ, Gómez-Leal A, López R: Mycotic keratitis in an eye care hospital in Mexico City. Rev Iberoam Micol 2010, 27:57-61.
• [46]Lewis R, Wiederhold N, Klepser M: In vitro pharmacodynamics of amphotericin B, itraconazole, and voriconazole against aspergillus, fusarium, and scedosporium spp. Antimicrob Agents Chemother 2005, 49:945-995.
• [47]Paphitou N, Ostrosky-Zeichner L, Paetznick V, Rodríguez J, Chen E, Rex J: In vitro activities of investigational triazoles against Fusarium species: effects of inoculum size and incubation time on broth microdilution susceptibility test results. Antimicrob Agents Chemother 2002, 46:3298-3300.
• [48]Pujol I, Guarro J, Gené J, Sala J: In-vitro antifungal susceptibility of clinical and environmental Fusarium spp. strains. J Antimicrob Chemother 1997, 39:163-167.
• [49]Oechsler R, Yamanaka T, Paulo Bispo J, Sartori J, Yu MC, Melo A, Miller D, Hofling-Lima A: Fusarium keratitis in Brazil: genotyping, in vitro susceptibilities, and clinical outcomes. Clin Ophthalmol 2013, 7:1693-1701.