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Early-Onset Invasive Infection Due to Corynespora cassiicola Associated with Compound Heterozygous CARD9 Mutations in a Colombian Patient

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Abstract

Purpose

CARD9 deficiency is an inborn error of immunity that predisposes otherwise healthy humans to mucocutaneous and invasive fungal infections, mostly caused by Candida, but also by dermatophytes, Aspergillus, and other fungi. Phaeohyphomycosis are an emerging group of fungal infections caused by dematiaceous fungi (phaeohyphomycetes) and are being increasingly identified in patients with CARD9 deficiency. The Corynespora genus belongs to phaeohyphomycetes and only one adult patient with CARD9 deficiency has been reported to suffer from invasive disease caused by C. cassiicola. We identified a Colombian child with an early-onset, deep, and destructive mucocutaneous infection due to C. cassiicola and we searched for mutations in CARD9.

Methods

We reviewed the medical records and immunological findings in the patient. Microbiologic tests and biopsies were performed. Whole-exome sequencing (WES) was made and Sanger sequencing was used to confirm the CARD9 mutations in the patient and her family. Finally, CARD9 protein expression was evaluated in peripheral blood mononuclear cells (PBMC) by western blotting.

Results

The patient was affected by a large, indurated, foul-smelling, and verrucous ulcerated lesion on the left side of the face with extensive necrosis and crusting, due to a C. cassiicola infectious disease. WES led to the identification of compound heterozygous mutations in the patient consisting of the previously reported p.Q289* nonsense (c.865C > T, exon 6) mutation, and a novel deletion (c.23_29del; p.Asp8Alafs10*) leading to a frameshift and a premature stop codon in exon 2. CARD9 protein expression was absent in peripheral blood mononuclear cells from the patient.

Conclusion

We describe here compound heterozygous loss-of-expression mutations in CARD9 leading to severe deep and destructive mucocutaneous phaeohyphomycosis due to C. cassiicola in a Colombian child.

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Acknowledgements

We are mostly grateful to the patient and her family for their participation in this study and to all the physicians who took part of the multidisciplinary team that took care of the child, for their invaluable support. We also thank Dr. Alexandro Bonifaz from the Dermatology Service at the General Hospital of Mexico for his helpful suggestions during the follow-up of the patient in Medellín and Karen Arango from the Corporación para las Investigaciones Biológicas (CIB) (Medellin, Colombia) for her assistance with the microbiologic results. Finally, we are thankful to the Primary Immunodeficiencies Foundation FIP for their assistance and financial support.

Funding

This work was supported by the Colombian Administrative Department of Science, Technology and Innovation (COLCIENCIAS, Código #111556934990, contract number 576-2013), ECOS-NORD (grant #619-2013), and Programa de Sostenibilidad Universidad de Antioquia 2017.

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Author notes

  1. Andrés Augusto Arias and José Luis Franco contributed equally to this work.

Authors and Affiliations

  1. Grupo de Inmunodeficiencias Primarias, Universidad de Antioquia UdeA, Calle 70 No. 52-21, Medellín, Colombia

    Carlos A. Arango-Franco, Marcela Moncada-Vélez, Sara Daniela Osorio, Lorena Castro, Julio Cesar Orrego, Andrés Augusto Arias & José Luis Franco

  2. Escuela de Microbiología, Universidad de Antioquia UdeA, Calle 70 No. 52-21, Medellín, Colombia

    Carlos A. Arango-Franco, Sara Daniela Osorio, Lorena Castro & Andrés Augusto Arias

  3. Departamento de Pediatría, Universidad de Antioquia UdeA, Calle 70 No. 52-21, Medellín, Colombia

    Claudia Patricia Beltrán & Carlos Garcés

  4. Medical and Experimental Mycology Group, Corporación para Investigaciones Biológicas (CIB), Medellín, Colombia

    Indira Berrío

  5. Hospital General de Medellín “Luz Castro de Gutiérrez” ESE, Medellín, Colombia

    Indira Berrío

  6. Infectología, Hospital Universitario Fernando Troconnis, Santa Marta, Colombia

    Cristian Mogollón

  7. Hospital Pablo Tobón Uribe, Medellín, Colombia

    Andrea Restrepo, Mónica Trujillo, Lina Vanessa Gómez, Verónica Molina, Delsy Yurledy del Río Cobaleda, Ana Cristina Ruiz & Carlos Garcés

  8. Servicio de Dermatología, Universidad Pontificia Bolivariana, Medellín, Colombia

    Lina Vanessa Gómez, Ana María Muñoz & Verónica Molina

  9. Centro Nacional de Secuenciación Genómica CNSG, Facultad de Medicina, Universidad de Antioquia UdeA, Calle 70 No 52-21, Medellín, Colombia

    Juan Fernando Alzate & Felipe Cabarcas

  10. Grupo SISTEMIC, Facultad de Ingeniería, Universidad de Antioquia UdeA , Calle 70 No 52-21, Medellín, Colombia

    Felipe Cabarcas

  11. Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM-U1163, Paris, EU, France

    Jean-Laurent Casanova, Jacinta Bustamante & Anne Puel

  12. Imagine Institute, Paris Descartes University, Paris, EU, France

    Jean-Laurent Casanova, Jacinta Bustamante & Anne Puel

  13. St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY, USA

    Jean-Laurent Casanova, Jacinta Bustamante & Anne Puel

  14. Pediatric Hematology-Immunology Unit, Necker Hospital for Sick Children, AP-HP, Paris, France

    Jean-Laurent Casanova

  15. Howard Hughes Medical Institute, New York, NY, USA

    Jean-Laurent Casanova

  16. Center for the Study of Primary Immunodeficiencies, Necker Hospital for Sick Children, Paris, EU, France

    Jacinta Bustamante

Authors
  1. Carlos A. Arango-Franco
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  2. Marcela Moncada-Vélez
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  22. Andrés Augusto Arias
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  23. José Luis Franco
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Contributions

JLF and AAA are the principal investigators and conceived the study. CAAF, SDO, and LC performed the experiments and took samples from the patient. JLC, AP, and JB contributed to the design of the study. JLF analyzed the flow cytometry data. MMV, JFA, AAA, and FC were responsible for genetic analysis. CPB, CM, AR, MT, LVG, AMM, VM, DYC, ACR, CG, IB, and JCO contributed to the collection of samples from the patients and provided a clinical oversight. IB contributed with the fungus identification. All authors revised the manuscript and approved the final manuscript. CAAF, AAA, JB, and JLF analyzed the results and wrote the manuscript.

Corresponding author

Correspondence to Andrés Augusto Arias.

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Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the local review board of the Universidad de Antioquia (F8790-07-0010) and conducted according to the “Scientific Standards for Technical and Administrative Health Research” established by the Colombian Ministry of Health Resolution 008430 of 1993. Informed consent was obtained from the patient or their family members included in this study.

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Arango-Franco, C.A., Moncada-Vélez, M., Beltrán, C.P. et al. Early-Onset Invasive Infection Due to Corynespora cassiicola Associated with Compound Heterozygous CARD9 Mutations in a Colombian Patient. J Clin Immunol 38, 794–803 (2018). https://doi.org/10.1007/s10875-018-0549-0

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