mycoses
Diagnosis,Therapy and Prophylaxis of Fungal Diseases
Short note
The pathogenic potential of the Lichtheimia genus revisited: Lichtheimia brasiliensis is a novel, non-pathogenic species Luiz C. M. de A. Santiago,4 Ilse D. Jacobsen3 and Kerstin Voigt1,2 Volker U. Schwartze,1,2,3 Andre 1 Jena Microbial Resource Collection, Leibniz Institute for Natural Product Research and Infection Biology – Hans Kno€ll Institute, Jena, Germany, 2Faculty of Biology and Pharmacy, Institute of Microbiology, Department Microbiology and Molecular Biology, Friedrich Schiller University Jena, Jena, Germany, 3 Microbial Immunology, Leibniz Institute for Natural Product Research and Infection Biology – Hans Kno€ll Institute, Jena, Germany and 4Federal Rural University of Pernambuco – Academic Unit of Serra Talhada, Pernambuco, Brazil
Summary
Lichtheimia brasiliensis was recently described as a novel species within the genus Lichtheimia, which comprises a total of six species. L. brasiliensis was first reported from soil in Brazil. The aim of the study was to determine the relative virulence potential of L. brasiliensis using an avian infection model based on chicken embryos.
Key words: Infection model, zygomycosis, Lichtheimia, virulence, pathogenesis, avian infection model.
Introduction Mucormycosis is a rare disease caused by fungi of the Mucorales order affecting immunocompromised hosts. The Mucorales genera most commonly isolated from patients are Mucor, Rhizomucor and Rhizopus.1–5 However, approximately 5% of mucormycoses worldwide are caused by Lichtheimia species.1 Within Europe, Lichtheimia species even range as the third to second most-common agent of mucormycosis.2,6 The genus Lichtheimia Vuill. (syn. Absidia pro parte, Mycocladus) consists of saprotrophic and predominantly thermotolerant species, which inhabit soil and decaying plant material. By 2010 five species of the genus were described: L. corymbifera (Cohn) Vuill. (syn. Absidia corymbifera, M. corymbifer), L. ramosa (Zopf) Vuill. (syn. A. ramosa, M. ramosus), L. hyalospora (syn. A. hyalospora, M. hyalosporus), L. ornata (A.K. Sarbhoy) Alastr.Izq. & Walther (syn. A. ornata) and L. sphaerocystis Alastr.-Izq. & Walther.7 Microscopically, these species are characterised by erect or slightly bent sporangiophores, apophysate collumellae, which frequently Correspondence: K. Voigt, Leibniz Institute for Natural Product Research €ll Institute, Jena Microbial Resource Coland Infection Biology – Hans Kno lection, Adolf-Reichwein-Strasse 23, D-07745 Jena, Germany. Tel.: +49 (0) 3641 532 1395. Fax: +49 (0) 3641 532 2395. E-mail: [email protected] Submitted for publication 1 August 2014 Revised 4 August 2014 Accepted for publication 4 August 2014
doi:10.1111/myc.12230
forms one to several projections. Giant cells are abundant. Suspensor cells of zygospores lack appendages. Equatorial rings surround occasionally the zygospores.8–10 Themotolerance is an important factor for differentiating Lichtheimia from Absidia. While Absidia is mesophilic and grows below 37 °C, Lichtheimia is thermotolerant having its optimum growth temperature at 37 °C.8 L. corymbifera and L. ramosa grow up to 49 °C, whereas the maximum growth temperature for L. ornata is 46 °C. Lichtheimia sphaerocystis and L. hyalospora grow at 37 and 40 °C, respectively, but fail to grow at temperatures above 40 °C.7 Recently, two specimens of a novel Lichtheimia species (L. brasiliensis A.L. Santiago Lima & Oliveira) were isolated from soil in semiarid and littoral dune areas in the northeast of Brazil.11 The strains were characterised based on the morphological, physiological and molecular data (5.8S and LSU rDNA sequences). In summary, it was found that the two isolates differ from all other Lichtheimia species by the formation of short, hemispherical, never spatulate or elliptical columellae, without projections. Occasionally, long conical or bell shaped apophyses are found. The colony and micromorphology of L. brasiliensis is shown in Fig. 1a. Both isolates grow better at 30–35 °C, with no growth at 42 °C, and giant cells are not observed.11 L. brasiliensis represents the most basal species of Lichtheimia, and can, therefore, be used to understand the evolution of phenotypic traits in Lichtheimia (Fig. 1b). Lichtheimia corymbifera, L. ramosa and L. ornata have been implicated in human infections and infection
© 2014 Blackwell Verlag GmbH Mycoses, 2014, 57 (Suppl. 3), 128–131
Virulence of Lichtheimia brasiliensis
(a)
(b)
Figure 1 (a) Macro- and micromorphol-
ogy of Lichtheimia brasiliensis: 1. Colony morphology; 2. Simple sporangiophore with an apophysate sporangium and rhizoid; 3. Sporangiospores. (b) Phylogenetic relationships among six species recognised within the genus Lichtheimia (modified after11). Clinically relevant species (L. corymbifera, L. ornata, L. ramosa) are highlighted in red, clinically non-relevant strains (L. sphaerocystis, L. hyalospora) are indicated in blue. L. brasiliensis is marked in grey because its clinical importance is still uncertain.
experiments using chicken embryos showed that the virulence potential of these species is higher than that of non-clinical species L. hyalospora and L. sphaerocystis.12 Furthermore, the virulence potential within the genus follows derived phylogenetic lineages (Fig. 1b). Consequently, the aim of this study was to determine the virulence potential of L. brasiliensis representing the most ancient lineage in order to test the evolution of pathogenicity within the genus Lichtheimia. A total of three strains comprising two strains of Lichtheimia brasiliensis URM 6910 and URM 6911 (JMRC:FSU:11614 and JMRC:FSU:11615, respectively)
© 2014 Blackwell Verlag GmbH Mycoses, 2014, 57 (Suppl. 3), 128–131
and one strain of L. corymbifera CBS 429.75 = ATCC 46771 (JMRC:FSU:9682) were used. The strains are deposited in the Jena Microbial Resource Collection (JMRC) Jena, Germany and the Centraalbureau voor Schimmelcultures (CBS) Utrecht, the Netherlands and the American Type Culture Collection (ATCC) USA as indicated above. To investigate the pathogenic potential of L. brasiliensis, embryonated chicken eggs were infected with spores from the sporangia of the strains as described previously.12–14 Briefly, all strains were grown on SUP medium15 (55 mmol l 1 glucose, 30 mmol l 1 potassium dihydrogen phosphate, 20 mmol l 1 ammonium
129
V. U. Schwartze et al.
(a)
(b)
Figure 2 Virulence of two representative
strains of Lichtheimia brasiliensis JMRC: FSU:11614 and JMRC:FSU:11615 and one strain (JMRC:FSU:9682) of L. corymbifera, which was used for reference purposes. Data are shown as Kaplan– Meyer curves. Survival of embryos infected with any strain was pairwise compared to survival of embryos infected with the reference strain L. corymbifera JMRC:FSU:9682 using the Log rank test with P < 0.01.
chloride, 5 mmol l 1 di-potassium hydrogen phosphate, 1 mmol l 1 magnesium sulphate and 0.5% yeast extract) at 37 °C for 7 days. Sporangiospores were harvested using sterile PBS (137 mmol l 1 NaCl, 10 mmol l 1 Na2HPO4, 2.7 mmol l 1 KCl, 1.76 mmol l 1 KH2PO4, pH7.4), washed three times with PBS, the spore concentrations were determined microscopically in a Thoma counting chamber and diluted to the concentrations with PBS as indicated in Fig. 2. Groups of twenty eggs per strain and dose were infected at developmental day 10 via the chorioallantoic membrane with 103 (Fig. 2a) and 104 (Fig. 2b) spores per egg in 100 ll sterile PBS. Survival was determined daily by candling. Infection with L. corymbifera resulted in 85% and 100% mortality at 104 and 103 spores per egg, respectively. The infection experiments were repeated minimum twice. In contrast, both strains of L. brasiliensis caused significantly less mortality in chicken embryos at both infection doses (Fig. 2). This is in accordance with previous findings that full virulence is restricted to three clinically relevant species.12 Previous studies showed that there may be a connection between the tolerance towards elevated
temperatures and the virulence potential of Lichtheimia species.7,12 To determine whether this correlation also occurred in L. brasiliensis, growth experiments were performed at different temperatures. Spore suspensions were prepared as described above and five ll of a 10-fold serial dilution series (107–104 spores ml 1) were spotted on solid medium of a square-shaped Petri dish containing SUP medium and incubated at 30, 37 and 42 °C for 24 h (Fig. 3). Experiments were performed in biological duplicates. Both strains of L. brasiliensis showed good growth at 30 and 37 °C, which is prerequisite for a successful pathogen in human and mammals (Fig. 3b,8). However, L. corymbifera showed faster growth at 37 °C and was still able to spread at 42 °C, while growth of L. brasiliensis was inhibited at 42 °C. Consequently, temperatures at or above 42 °C appear to be suppressive for the non-clinically relevant or not human pathogenic species, which are L. brasiliensis, L. hyalospora and L. sphaerocystis.7,12 Our results show that L. brasiliensis, the most basal species of Lichtheimia, represents a non-pathogenic member of this genus. Thus, the higher virulence
Figure 3 Droplet assay displays growth behaviour on three different temperatures: 30, 37 and 42 °C. Five microlitres of spore suspen-
sions were dropped in 10-fold serial dilution series containing 107, 106, 105 and 104 spores ml 1. This means that 50 000; 5000; 500 and 50 spores (from left to right) were spotted on solid medium of a square-shaped Petri dish containing SUP medium and incubated at 30, 37 and 42 °C for 24 h.
130
© 2014 Blackwell Verlag GmbH Mycoses, 2014, 57 (Suppl. 3), 128–131
Virulence of Lichtheimia brasiliensis
potential of the three clinically relevant Lichtheimia species likely developed during evolution after the ancestor of L. corymbifera, L. ramosa and L. ornata branched off the basal lineages (Fig. 1).
3
4
Acknowledgment ALCMdeAS thanks the Programa de P os-graduacß~ ao em Biologia de Fungos, Universidade Federal de Pernambuco, Recife, PE, Brazil for financial support. KV and VUS are grateful for financial support by the University of Jena. The virulence tests were partially supported by the Leibniz Institute for Natural Product Research and Infection Biology – Hans Knoell Institute (HKI) Jena Germany and by the Deutsche Forschungsgemeinschaft (DFG) (Collaborative Research Center/ Transregio CRC/TR 124 FungiNet, project Z1 to KV). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
5
6
7
8
9 10 11
Conflict of interest The authors declare that no conflict of interest exists.
12 13
References 14 1
2
Roden MM, Zaoutis TE, Buchanan WL et al. Epidemiology and outcome of zygomycosis: a review of 929 reported cases. Clin Infect Dis 2005; 41: 634–53. Skiada A, Pagano L, Groll A et al. Zygomycosis in Europe: analysis of 230 cases accrued by the registry of the European Confederation
© 2014 Blackwell Verlag GmbH Mycoses, 2014, 57 (Suppl. 3), 128–131
15
of Medical Mycology (ECMM) Working Group on Zygomycosis between 2005 and 2007. Clin Microbiol Infect 2011; 17: 1859–67. Greenberg RN, Scott LJ, Vaughn HH, Ribes JA. Zygomycosis (mucormycosis): emerging clinical importance and new treatments. Curr Opin Infect Dis 2004; 17: 517–25. Gomes MZR, Lewis RE, Kontoyiannis DP. Mucormycosis caused by unusual mucormycetes, non-Rhizopus, -Mucor, and -Lichtheimia species. Clin Microbiol Rev 2011; 24: 411–45. Schwarz P, Bretagne S, Gantier J et al. Molecular identification of zygomycetes from culture and experimentally infected tissues. J Clin Microbiol 2006; 44: 340–9. Lanternier F, Dannaoui E, Morizot G et al. A global analysis of mucormycosis in France: the RetroZygo Study (2005-2007). Clin Infect Dis 2012; 54(Suppl. 1): S35–43. Alastruey-Izquierdo A, Hoffmann K, de Hoog GS et al. Species recognition and clinical relevance of the zygomycetous genus Lichtheimia (syn. Absidia pro parte, Mycocladus). J Clin Microbiol 2010; 48: 2154–70. Hoffmann K, Discher S, Voigt K. Revision of the genus Absidia (Mucorales, Zygomycetes) based on physiological, phylogenetic, and morphological characters; thermotolerant Absidia spp. form a coherent group, Mycocladiaceae fam. nov. Mycol Res 2007; 111: 1169–83. Ellis J, Hesseltine C. Species of Absidia with ovoid sporangiospores. II. Sabouraudia 1966; 5: 59–77. Hesseltine C, Ellis J. Species of Absidia with ovoid sporangiospores. I. Mycologia 1966; 58: 761–85. Santiago ALCM, Hoffmann K, Lima DX et al. A new species of Lichtheimia (Mucoromycotina, Mucorales) isolated from Brazilian soil. Mycol Prog 2013; 12: 343–352. Schwartze VU, Hoffmann K, Nyilasi I et al. Lichtheimia species exhibit differences in virulence potential. PLoS ONE 2012; 7: e40908. H€ artl A, Hillesheim HG, Kunkel W, Schrinner EJ. The Candida infected hen’s egg. An alternative test system for systemic anticandida activity. Arzneimittelforschung 1995; 45: 926–8. Jacobsen ID, Grosse K, Slesiona S et al. Embryonated eggs as an alternative infection model to investigate Aspergillus fumigatus virulence. Infect Immun 2010; 78: 2995–3006. W€ ostemeyer J. Strain-dependent variation in ribosomal DNA arrangement in Absidia glauca. Eur J Biochem 1985; 146: 443–8.
131
Copyright of Mycoses is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
Diagnosis,Therapy and Prophylaxis of Fungal Diseases
Short note
The pathogenic potential of the Lichtheimia genus revisited: Lichtheimia brasiliensis is a novel, non-pathogenic species Luiz C. M. de A. Santiago,4 Ilse D. Jacobsen3 and Kerstin Voigt1,2 Volker U. Schwartze,1,2,3 Andre 1 Jena Microbial Resource Collection, Leibniz Institute for Natural Product Research and Infection Biology – Hans Kno€ll Institute, Jena, Germany, 2Faculty of Biology and Pharmacy, Institute of Microbiology, Department Microbiology and Molecular Biology, Friedrich Schiller University Jena, Jena, Germany, 3 Microbial Immunology, Leibniz Institute for Natural Product Research and Infection Biology – Hans Kno€ll Institute, Jena, Germany and 4Federal Rural University of Pernambuco – Academic Unit of Serra Talhada, Pernambuco, Brazil
Summary
Lichtheimia brasiliensis was recently described as a novel species within the genus Lichtheimia, which comprises a total of six species. L. brasiliensis was first reported from soil in Brazil. The aim of the study was to determine the relative virulence potential of L. brasiliensis using an avian infection model based on chicken embryos.
Key words: Infection model, zygomycosis, Lichtheimia, virulence, pathogenesis, avian infection model.
Introduction Mucormycosis is a rare disease caused by fungi of the Mucorales order affecting immunocompromised hosts. The Mucorales genera most commonly isolated from patients are Mucor, Rhizomucor and Rhizopus.1–5 However, approximately 5% of mucormycoses worldwide are caused by Lichtheimia species.1 Within Europe, Lichtheimia species even range as the third to second most-common agent of mucormycosis.2,6 The genus Lichtheimia Vuill. (syn. Absidia pro parte, Mycocladus) consists of saprotrophic and predominantly thermotolerant species, which inhabit soil and decaying plant material. By 2010 five species of the genus were described: L. corymbifera (Cohn) Vuill. (syn. Absidia corymbifera, M. corymbifer), L. ramosa (Zopf) Vuill. (syn. A. ramosa, M. ramosus), L. hyalospora (syn. A. hyalospora, M. hyalosporus), L. ornata (A.K. Sarbhoy) Alastr.Izq. & Walther (syn. A. ornata) and L. sphaerocystis Alastr.-Izq. & Walther.7 Microscopically, these species are characterised by erect or slightly bent sporangiophores, apophysate collumellae, which frequently Correspondence: K. Voigt, Leibniz Institute for Natural Product Research €ll Institute, Jena Microbial Resource Coland Infection Biology – Hans Kno lection, Adolf-Reichwein-Strasse 23, D-07745 Jena, Germany. Tel.: +49 (0) 3641 532 1395. Fax: +49 (0) 3641 532 2395. E-mail: [email protected] Submitted for publication 1 August 2014 Revised 4 August 2014 Accepted for publication 4 August 2014
doi:10.1111/myc.12230
forms one to several projections. Giant cells are abundant. Suspensor cells of zygospores lack appendages. Equatorial rings surround occasionally the zygospores.8–10 Themotolerance is an important factor for differentiating Lichtheimia from Absidia. While Absidia is mesophilic and grows below 37 °C, Lichtheimia is thermotolerant having its optimum growth temperature at 37 °C.8 L. corymbifera and L. ramosa grow up to 49 °C, whereas the maximum growth temperature for L. ornata is 46 °C. Lichtheimia sphaerocystis and L. hyalospora grow at 37 and 40 °C, respectively, but fail to grow at temperatures above 40 °C.7 Recently, two specimens of a novel Lichtheimia species (L. brasiliensis A.L. Santiago Lima & Oliveira) were isolated from soil in semiarid and littoral dune areas in the northeast of Brazil.11 The strains were characterised based on the morphological, physiological and molecular data (5.8S and LSU rDNA sequences). In summary, it was found that the two isolates differ from all other Lichtheimia species by the formation of short, hemispherical, never spatulate or elliptical columellae, without projections. Occasionally, long conical or bell shaped apophyses are found. The colony and micromorphology of L. brasiliensis is shown in Fig. 1a. Both isolates grow better at 30–35 °C, with no growth at 42 °C, and giant cells are not observed.11 L. brasiliensis represents the most basal species of Lichtheimia, and can, therefore, be used to understand the evolution of phenotypic traits in Lichtheimia (Fig. 1b). Lichtheimia corymbifera, L. ramosa and L. ornata have been implicated in human infections and infection
© 2014 Blackwell Verlag GmbH Mycoses, 2014, 57 (Suppl. 3), 128–131
Virulence of Lichtheimia brasiliensis
(a)
(b)
Figure 1 (a) Macro- and micromorphol-
ogy of Lichtheimia brasiliensis: 1. Colony morphology; 2. Simple sporangiophore with an apophysate sporangium and rhizoid; 3. Sporangiospores. (b) Phylogenetic relationships among six species recognised within the genus Lichtheimia (modified after11). Clinically relevant species (L. corymbifera, L. ornata, L. ramosa) are highlighted in red, clinically non-relevant strains (L. sphaerocystis, L. hyalospora) are indicated in blue. L. brasiliensis is marked in grey because its clinical importance is still uncertain.
experiments using chicken embryos showed that the virulence potential of these species is higher than that of non-clinical species L. hyalospora and L. sphaerocystis.12 Furthermore, the virulence potential within the genus follows derived phylogenetic lineages (Fig. 1b). Consequently, the aim of this study was to determine the virulence potential of L. brasiliensis representing the most ancient lineage in order to test the evolution of pathogenicity within the genus Lichtheimia. A total of three strains comprising two strains of Lichtheimia brasiliensis URM 6910 and URM 6911 (JMRC:FSU:11614 and JMRC:FSU:11615, respectively)
© 2014 Blackwell Verlag GmbH Mycoses, 2014, 57 (Suppl. 3), 128–131
and one strain of L. corymbifera CBS 429.75 = ATCC 46771 (JMRC:FSU:9682) were used. The strains are deposited in the Jena Microbial Resource Collection (JMRC) Jena, Germany and the Centraalbureau voor Schimmelcultures (CBS) Utrecht, the Netherlands and the American Type Culture Collection (ATCC) USA as indicated above. To investigate the pathogenic potential of L. brasiliensis, embryonated chicken eggs were infected with spores from the sporangia of the strains as described previously.12–14 Briefly, all strains were grown on SUP medium15 (55 mmol l 1 glucose, 30 mmol l 1 potassium dihydrogen phosphate, 20 mmol l 1 ammonium
129
V. U. Schwartze et al.
(a)
(b)
Figure 2 Virulence of two representative
strains of Lichtheimia brasiliensis JMRC: FSU:11614 and JMRC:FSU:11615 and one strain (JMRC:FSU:9682) of L. corymbifera, which was used for reference purposes. Data are shown as Kaplan– Meyer curves. Survival of embryos infected with any strain was pairwise compared to survival of embryos infected with the reference strain L. corymbifera JMRC:FSU:9682 using the Log rank test with P < 0.01.
chloride, 5 mmol l 1 di-potassium hydrogen phosphate, 1 mmol l 1 magnesium sulphate and 0.5% yeast extract) at 37 °C for 7 days. Sporangiospores were harvested using sterile PBS (137 mmol l 1 NaCl, 10 mmol l 1 Na2HPO4, 2.7 mmol l 1 KCl, 1.76 mmol l 1 KH2PO4, pH7.4), washed three times with PBS, the spore concentrations were determined microscopically in a Thoma counting chamber and diluted to the concentrations with PBS as indicated in Fig. 2. Groups of twenty eggs per strain and dose were infected at developmental day 10 via the chorioallantoic membrane with 103 (Fig. 2a) and 104 (Fig. 2b) spores per egg in 100 ll sterile PBS. Survival was determined daily by candling. Infection with L. corymbifera resulted in 85% and 100% mortality at 104 and 103 spores per egg, respectively. The infection experiments were repeated minimum twice. In contrast, both strains of L. brasiliensis caused significantly less mortality in chicken embryos at both infection doses (Fig. 2). This is in accordance with previous findings that full virulence is restricted to three clinically relevant species.12 Previous studies showed that there may be a connection between the tolerance towards elevated
temperatures and the virulence potential of Lichtheimia species.7,12 To determine whether this correlation also occurred in L. brasiliensis, growth experiments were performed at different temperatures. Spore suspensions were prepared as described above and five ll of a 10-fold serial dilution series (107–104 spores ml 1) were spotted on solid medium of a square-shaped Petri dish containing SUP medium and incubated at 30, 37 and 42 °C for 24 h (Fig. 3). Experiments were performed in biological duplicates. Both strains of L. brasiliensis showed good growth at 30 and 37 °C, which is prerequisite for a successful pathogen in human and mammals (Fig. 3b,8). However, L. corymbifera showed faster growth at 37 °C and was still able to spread at 42 °C, while growth of L. brasiliensis was inhibited at 42 °C. Consequently, temperatures at or above 42 °C appear to be suppressive for the non-clinically relevant or not human pathogenic species, which are L. brasiliensis, L. hyalospora and L. sphaerocystis.7,12 Our results show that L. brasiliensis, the most basal species of Lichtheimia, represents a non-pathogenic member of this genus. Thus, the higher virulence
Figure 3 Droplet assay displays growth behaviour on three different temperatures: 30, 37 and 42 °C. Five microlitres of spore suspen-
sions were dropped in 10-fold serial dilution series containing 107, 106, 105 and 104 spores ml 1. This means that 50 000; 5000; 500 and 50 spores (from left to right) were spotted on solid medium of a square-shaped Petri dish containing SUP medium and incubated at 30, 37 and 42 °C for 24 h.
130
© 2014 Blackwell Verlag GmbH Mycoses, 2014, 57 (Suppl. 3), 128–131
Virulence of Lichtheimia brasiliensis
potential of the three clinically relevant Lichtheimia species likely developed during evolution after the ancestor of L. corymbifera, L. ramosa and L. ornata branched off the basal lineages (Fig. 1).
3
4
Acknowledgment ALCMdeAS thanks the Programa de P os-graduacß~ ao em Biologia de Fungos, Universidade Federal de Pernambuco, Recife, PE, Brazil for financial support. KV and VUS are grateful for financial support by the University of Jena. The virulence tests were partially supported by the Leibniz Institute for Natural Product Research and Infection Biology – Hans Knoell Institute (HKI) Jena Germany and by the Deutsche Forschungsgemeinschaft (DFG) (Collaborative Research Center/ Transregio CRC/TR 124 FungiNet, project Z1 to KV). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
5
6
7
8
9 10 11
Conflict of interest The authors declare that no conflict of interest exists.
12 13
References 14 1
2
Roden MM, Zaoutis TE, Buchanan WL et al. Epidemiology and outcome of zygomycosis: a review of 929 reported cases. Clin Infect Dis 2005; 41: 634–53. Skiada A, Pagano L, Groll A et al. Zygomycosis in Europe: analysis of 230 cases accrued by the registry of the European Confederation
© 2014 Blackwell Verlag GmbH Mycoses, 2014, 57 (Suppl. 3), 128–131
15
of Medical Mycology (ECMM) Working Group on Zygomycosis between 2005 and 2007. Clin Microbiol Infect 2011; 17: 1859–67. Greenberg RN, Scott LJ, Vaughn HH, Ribes JA. Zygomycosis (mucormycosis): emerging clinical importance and new treatments. Curr Opin Infect Dis 2004; 17: 517–25. Gomes MZR, Lewis RE, Kontoyiannis DP. Mucormycosis caused by unusual mucormycetes, non-Rhizopus, -Mucor, and -Lichtheimia species. Clin Microbiol Rev 2011; 24: 411–45. Schwarz P, Bretagne S, Gantier J et al. Molecular identification of zygomycetes from culture and experimentally infected tissues. J Clin Microbiol 2006; 44: 340–9. Lanternier F, Dannaoui E, Morizot G et al. A global analysis of mucormycosis in France: the RetroZygo Study (2005-2007). Clin Infect Dis 2012; 54(Suppl. 1): S35–43. Alastruey-Izquierdo A, Hoffmann K, de Hoog GS et al. Species recognition and clinical relevance of the zygomycetous genus Lichtheimia (syn. Absidia pro parte, Mycocladus). J Clin Microbiol 2010; 48: 2154–70. Hoffmann K, Discher S, Voigt K. Revision of the genus Absidia (Mucorales, Zygomycetes) based on physiological, phylogenetic, and morphological characters; thermotolerant Absidia spp. form a coherent group, Mycocladiaceae fam. nov. Mycol Res 2007; 111: 1169–83. Ellis J, Hesseltine C. Species of Absidia with ovoid sporangiospores. II. Sabouraudia 1966; 5: 59–77. Hesseltine C, Ellis J. Species of Absidia with ovoid sporangiospores. I. Mycologia 1966; 58: 761–85. Santiago ALCM, Hoffmann K, Lima DX et al. A new species of Lichtheimia (Mucoromycotina, Mucorales) isolated from Brazilian soil. Mycol Prog 2013; 12: 343–352. Schwartze VU, Hoffmann K, Nyilasi I et al. Lichtheimia species exhibit differences in virulence potential. PLoS ONE 2012; 7: e40908. H€ artl A, Hillesheim HG, Kunkel W, Schrinner EJ. The Candida infected hen’s egg. An alternative test system for systemic anticandida activity. Arzneimittelforschung 1995; 45: 926–8. Jacobsen ID, Grosse K, Slesiona S et al. Embryonated eggs as an alternative infection model to investigate Aspergillus fumigatus virulence. Infect Immun 2010; 78: 2995–3006. W€ ostemeyer J. Strain-dependent variation in ribosomal DNA arrangement in Absidia glauca. Eur J Biochem 1985; 146: 443–8.
131
Copyright of Mycoses is the property of Wiley-Blackwell and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
