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STEM CELL TRANSPLANTATION

Disturbances in microbial skin recolonization and cutaneous immune response following allogeneic stem cell transfer

Leukemia volume 36, pages 2705–2714 (2022)Cite this article

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A Correction to this article was published on 14 February 2023

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Abstract

The composition of the gut microbiome influences the clinical course after allogeneic hematopoietic stem cell transplantation (HSCT), but little is known about the relevance of skin microorganisms. In a single-center, observational study, we recruited a cohort of 50 patients before undergoing conditioning treatment and took both stool and skin samples up to one year after HSCT. We could confirm intestinal dysbiosis following HSCT and report that the skin microbiome is likewise perturbed in HSCT-recipients. Overall bacterial colonization of the skin was decreased after conditioning. Particularly patients that developed acute skin graft-versus-host disease (aGVHD) presented with an overabundance of Staphylococcus spp. In addition, a loss in alpha diversity was indicative of aGVHD development already before disease onset and correlated with disease severity. Further, co-localization of CD45+ leukocytes and staphylococci was observed in the skin of aGVHD patients even before disease development and paralleled with upregulated genes required for antigen-presentation in mononuclear phagocytes. Overall, our data reveal disturbances of the skin microbiome as well as cutaneous immune response in HSCT recipients with changes associated with cutaneous aGVHD.

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Fig. 1: Conditioning regimen induces changes in stool and skin microbiome.
Fig. 2: Low alpha diversity and Staphylococcus overgrowth in skin aGVHD.
Fig. 3: Functional analysis of Staphylococcus spp. from lesional/ non-lesional skin.
Fig. 4: Bacterial FISH reveals changes in skin colonization after conditioning.
Fig. 5: Activation of host immunity via conditioning therapy.

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Data availability

16S rRNA gene amplicon and whole-genome sequencing data are available under the BioProject accession number PRJNA804670. Bulk RNA sequencing data are deposited in NCBI’s Gene Expression Omnibus database (GSE198625).

Code availability

The code for the co-localization score is available via https://github.com/ramvinay/HostMicrobiome.

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Acknowledgements

We thank the Joint Microbiome Facility of the Medical University of Vienna and the University of Vienna as well as Biomedical Sequencing Facility (BSF) at CeMM for assistance with next-generation sequencing. This work was supported by funds of the Austrian Science Fund (FWF, P31494), the Oesterreichische Nationalbank (Austrian Central Bank; Anniversary Fund; project number, 17872), and by the Innovation Fund of the Austrian Academy of Sciences (ÖAW; project number, IF_2017_29). NB was supported by the ESCMID Research Grant 2020 of the European Society of Clinical Microbiology and Infectious Diseases. SK received funding from the Austrian Science Fund, FWF, via the Doctoral Program Cell Communication in Health and Disease (W 1205-B09), and the Special Research Programs Chromatin Landscapes (F6104) and Immunothrombosis (F5410).

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Authors and Affiliations

  1. Department of Dermatology, Medical University of Vienna, 1090, Vienna, Austria

    Nadine Bayer, Ram Vinay Pandey, Laura-Marie Gail, Johanna Strobl, Luisa Unterluggauer, Anna Redl, Victoria Bachmayr, Lisa Kleissl, Lukas Hammerl & Georg Stary

  2. CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, 1090, Vienna, Austria

    Nadine Bayer, Florian Deckert, Laura-Marie Gail, Johanna Strobl, Anna Redl & Georg Stary

  3. Joint Microbiome Facility of the Medical University of Vienna and the University of Vienna, 1030, Vienna, Austria

    Bela Hausmann, Petra Pjevac, Rasmus Kirkegaard & David Berry

  4. Division of Clinical Microbiology, Department of Laboratory Medicine, Medical University of Vienna, 1090, Vienna, Austria

    Bela Hausmann, Marion Nehr & Athanasios Makristathis

  5. Department of Medicine I, Laboratory of Infection Biology, Medical University of Vienna, 1090, Vienna, Austria

    Florian Deckert & Sylvia Knapp

  6. Ludwig Boltzmann Institute for Rare and Undiagnosed Diseases, 1090, Vienna, Austria

    Laura-Marie Gail, Lisa Kleissl & Georg Stary

  7. Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, Centre for Microbiology and Environmental Systems Science, University of Vienna, 1030, Vienna, Austria

    Petra Pjevac, Rasmus Kirkegaard & David Berry

  8. Centre for Medical Statistics, Informatics, and Intelligent Systems, Medical University of Vienna, 1090, Vienna, Austria

    Christoph Krall

  9. Department of Biomedical Imaging and Image-guided Therapy, Medical University of Vienna, Vienna, Austria

    Martin L. Watzenboeck

  10. TissueGnostics GmbH, 1020, Vienna, Austria

    Robert Nica & Rupert C. Ecker

  11. Division of Plastic and Reconstructive Surgery, Department of Surgery, Medical University of Vienna, 1090, Vienna, Austria

    Clement Staud

  12. Department of Internal Medicine I, Hematopoietic Stem Cell Transplantation Unit, Medical University of Vienna, 1090, Vienna, Austria

    Philipp Wohlfarth & Werner Rabitsch

  13. School of Biomedical Sciences, Faculty of Health, Queensland University of Technology, Brisbane, QLD 4059, Australia

    Rupert C. Ecker

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  1. Nadine Bayer
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Contributions

Conceptualization, GS; Methodology, NB; Software, RN and MLW; Formal Analysis, NB, BH, RVP, FD, PP, CK and RK; Investigation, NB, LMG, JS, AR, VB, LK, MN and LH; Resources, CS, PW and WR; Data Curation, NB, BH and LU; Writing—Original Draft, NB.; Writing—Review and Editing, GS, SK; DB and AM; Visualization, NB; Supervision, GS, SK; DB and RCE; Funding Acquisition, GS, NB.

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Correspondence to Georg Stary.

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Bayer, N., Hausmann, B., Pandey, R.V. et al. Disturbances in microbial skin recolonization and cutaneous immune response following allogeneic stem cell transfer. Leukemia 36, 2705–2714 (2022). https://doi.org/10.1038/s41375-022-01712-z

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