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Cladosporium halotolerans: Exploring an Unheeded Human Pathogen

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Abstract

Background

Cladosporium halotolerans is a saprobic fungus, rarely implicated in human infections. The identification is challenging due to non-specific phenotypic features.

Objective

To decipher clinical spectrum, microbiological and susceptibility profile of clinical and environmental isolates of Cladosporium halotolerans.

Method

All the isolates identified as Cladosporium halotolerans deposited in National Culture Collection for Pathogenic Fungi (NCCPF), Postgraduate Institute of Medical Education and Research, Chandigarh, India were revived. Phenotypic and molecular characterization targeting internal transcribed spacer (ITS) region of ribosomal DNA, large subunit of ribosomal DNA (LSU; NL1 and NL4), actin (ACT) and beta-tubulin (TUB) was done. Scanning electron microscopy (SEM) was performed to determine any phenotypic variations. Antifungal susceptibility testing (AFST) was carried out for eight antifungal agents as per CLSI M38 Ed3 guidelines. We also performed systematic literature review of all the cases of Cladosporium halotolerans reported till date.

Results

A total of four isolates (clinical, n = 3; soil, n = 1) identified as Cladosporium halotolerans were included in the study. The clinical sites were skin, maxillary tissue and nail. All patients were apparently immunocompetent, and history of trauma was recorded in one patient. All patients improved on antifungal therapy. The cultures revealed growth of black mycelial fungus and microscopic examination demonstrated dematiaceous septate hyphae with erect conidiophores and conidia in branched acropetal chains. Based on molecular methods, all the four isolates were identified as C. halotolerans. SEM revealed no variation in length and width of the conidia, conidiophores, ramoconidium and hyphae among the isolates. All molecular targets, such as ITS region, LSU (partially sequenced), ACT and TUB were able to differentiate the isolates. Minimum inhibitory concentrations for antifungals were: triazoles (0.12–2 μg/ml), amphotericin B (4 μg/ml) and echinocandins (2–8 μg/ml).

Conclusion

We report role of the rarely isolated dematiaceous fungus, C. halotolerans, in causing human infections. The study emphasizes the role of molecular methods in precisely identifying these species. Triazoles are more active against these black fungi compared to polyenes or echinocandins.

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References

  1. Crous PW, Shivas RG, Quaedvlieg W, van der Bank M, Zhang Y, Summerell BA, et al. Fungal planet description sheets: 214–280. Persoonia. 2014;32:184–306.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bensch K, Braun U, Groenewald JZ, Crous PW. The genus Cladospoirum. Stud Mycol. 2012;72:1–401.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Frasz SL, Miller JD. Fungi in ontario maple syrup & some factors that determine the presence of mold damage. Int J Food Microbiol. 2015;207:66–70.

    Article  CAS  PubMed  Google Scholar 

  4. Köhl J, Scheer C, Holb IJ, Masny S, Molhoek W. Toward an integrated use of biological control by Cladosporium cladosporioides H39 in apple scab (Venturia inaequalis) management. Plant Dis. 2015;99:535–43.

    Article  PubMed  Google Scholar 

  5. Segers FJJ, van Laarhoven KA, Huinink HP, Adan OCG, Wösten HAB, Dijksterhuis J. The indoor fungus Cladosporium halotolerans survives humidity dynamics markedly better than Aspergillus niger and Penicillium rubens despite less growth at lowered steady-state water activity. Appl Environ Microbiol. 2016;82:5089–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. David JC. A Contribution to the systematics of Cladosporium: revision of the fungi previously referred to Heterosporium. Wallingford: CAB International; 1997. p. 157.

    Google Scholar 

  7. Sandoval-Denis M, Gené J, Sutton DA, Wiederhold NP, Cano-Lira JF, Guarro J. New species of Cladosporium associated with human and animal infections. Persoonia. 2016;36:281–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Cheng SCH, Lin YY, Kuo CN, Lai LJ. Cladosporium keratitis—a case report and literature review. BMC Ophthalmol. 2015;15:106.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Crous PW, Braun U, Schubert K, Groenewald JZ. Delimiting Cladosporium from morphologically similar genera. Stud Mycol. 2007;58:33–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Sandoval-Denis M, Sutton DA, Martin-Vicente A, Cano-Lira JF, Wiederhold N, Guarro J, et al. Cladosporium species recovered from clinical samples in the United States. J Clin Microbiol. 2015;53:2990–3000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Sellart-Altisent M, Torres-Rodríguez JM, Gómez de Ana S, Alvarado-Ramírez E. Microbiota fúngica nasal en sujetos alérgicos y sanos [nasal fungal microbiota in allergic and healthy subjects]. Rev Iberoam Micol. 2007;24:125–30.

    Article  PubMed  Google Scholar 

  12. Drabick JJ, Gomatos PJ, Solis JB. Cutaneous cladosporiosis as a complication of skin testing in a man positive for human immunodeficiency virus. J Am Acad Dermatol. 1990;22:135–6.

    Article  CAS  PubMed  Google Scholar 

  13. Gugnani HC, Ramesh V, Sood N, Guarro J, Moin-Ul-Haq P-J, et al. Cutaneous phaeohyphomycosis caused by Cladosporium oxysporum and its treatment with potassium iodide. Med Mycol. 2006;44:285.

    Article  CAS  PubMed  Google Scholar 

  14. Gugnani HC, Sood N, Singh B, Makkar R. Case report. Subcutaneous phaeohyphomycosis due to Cladosporium cladosporioides. Mycoses. 2000;43:85–7.

    Article  CAS  PubMed  Google Scholar 

  15. Sang H, Zheng XE, Zhou WQ, He W, Lv GX, Shen YN, et al. A case of subcutaneous phaeohyphomycosis caused by Cladosporium cladosporioides and its treatment. Mycoses. 2012;55:195–7.

    Article  CAS  PubMed  Google Scholar 

  16. Kaur H, Rudramurthy SM, Mohindra S, Gupta S, Chakrabarti A. Ochroconis humicola coexisting with esthesioneuroblastoma: an incidental coloniser or allergen? Mycopathologia. 2014;178:79–83.

    Article  PubMed  Google Scholar 

  17. Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA, McWilliam H, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23:2947–8.

    Article  CAS  PubMed  Google Scholar 

  18. Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021;38:3022–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. M38Ed3 Filamentous Fungi Antifungal Susceptibility Test [Internet]. Clinical & Laboratory Standards Institute. [cited 2022 Jul 21]. Available from: https://clsi.org/standards/products/microbiology/documents/m38/.

  20. Kantarcioglu AS, Yücel A, de Hoog GS. Case report. Isolation of Cladosporium cladosporoides from cerebrospinal fluid. Mycoses. 2002;45:500–3.

    CAS  PubMed  Google Scholar 

  21. de Hoog GS, Guého E, Masclaux F, Gerrits van den Ende AH, Kwon-Chung KJ, McGinnis MR. Nutritional physiology and taxonomy of human-pathogenic Cladosporium-Xylohypha species. J Med Vet Mycol. 1995;33:339–47.

    Article  PubMed  Google Scholar 

  22. Lalueza A, López-Medrano F, del Palacio A, Alhambra A, Alvarez E, Ramos A, et al. Cladosporium macrocarpum brain abscess after endoscopic ultrasound-guided celiac plexus block. Endoscopy. 2011;43(Suppl 2):E9–10.

    Article  PubMed  Google Scholar 

  23. Bentz MS, Sautter RL. Disseminated infection with Aspergillus fumigatus and Cladosporium cladosporioides in an immunocompromised host, abstr F-37. Abstr 93rd Gen Meet Am Soc Microbiol. Washington: American Society for Microbiology; 1993. p. 533.

    Google Scholar 

  24. Deng S, de Hoog GS, Badali H, Yang L, Najafzadeh MJ, et al. In vitro antifungal susceptibility of Cladophialophora carrionii, an agent of human chromoblastomycosis. Antimicrob Agents Chemother. 2013;57:1974–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Chakrabarti A, Kaur H, Rudramurthy SM, Appannanavar SB, Patel A, Mukherjee KK, et al. Brain abscess due to Cladophialophora bantiana: a review of 124 cases. Med Mycol. 2016;54:111–9.

    Article  PubMed  Google Scholar 

  26. Sosa EE, Cohen PR, Tschen JA. Cladosporium scalp infection. Skinmed. 2012;10:393–4.

    PubMed  Google Scholar 

  27. Vieira MR, Milheiro A, Pacheco FA. Phaeohyphomycosis due to Cladosporium cladosporioides. Med Mycol. 2001;39:135–7.

    Article  CAS  PubMed  Google Scholar 

  28. Yano S, Koyabashi K, Kato K. Intrabronchial lesion due to Cladosporium sphaerospermum in a healthy, non-asthmatic woman. Mycoses. 2003;46:348–50.

    Article  CAS  PubMed  Google Scholar 

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Funding

We gratefully acknowledge the Department of Science and Technology-Science and Engineering Research Board (DST-SERB), New Delhi for extending financial support to carry out this research vide sanction number EMR/2017/003448 dated 03-10-2018.

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Authors and Affiliations

Authors

Contributions

HK: Supervision, study design, manuscript writing and editing; PG: Data collection, data analysis, review of literature, manuscript writing; HA: Data collection, experiments, phylogenetic analysis; SAS: experiments, phylogenetic analysis; SS: Data collection; SSahu: Data collection; KT: Data collection; TN: Data collection, patient management, manuscript editing; SG: Experiment supervision; AG: Experiment Supervision and manuscript editing; SMR: Study design, experiment designing, reviewing of manuscript, supervision.

Corresponding author

Correspondence to Shivaprakash M. Rudramurthy.

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Conflict of interest

The authors have reported no conflicts of interest.

Ethical Approval

The study was approved by Institute Ethics Committee vide number IEC-04/2018-927.

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Kaur, H., Gupta, P., Ahmad, H. et al. Cladosporium halotolerans: Exploring an Unheeded Human Pathogen. Mycopathologia 188, 1027–1040 (2023). https://doi.org/10.1007/s11046-023-00801-6

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  • DOI: https://doi.org/10.1007/s11046-023-00801-6

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