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

Nadine Bayer; Bela Hausman; Ram Vinay Pandey; Florian Deckert; Laura Marie Gail; Johanna Strobl; Petra Pjevac; Christoph Krall; Luisa Unterluggauer; Anna Redl; Victoria Bachmayr; Lisa Kleissl; Marion Nehr; Rasmus Kirkegaard; Athanasios Makristathis; Martin L. Watzenboeck; Robert Nica; Clement Staud; Lukas Hammerl; Philipp Wohlfarth; Rupert C. Ecker; Sylvia Knapp; Werner Rabitsch; David Berry; Georg Stary

doi:10.1038/s41375-022-01712-z

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

Nadine Bayer, Bela Hausman, Ram Vinay Pandey, Florian Deckert, Laura Marie Gail, Johanna Strobl, Petra Pjevac, Christoph Krall, Luisa Unterluggauer, Anna Redl, Victoria Bachmayr, Lisa Kleissl, Marion Nehr, Rasmus Kirkegaard, Athanasios Makristathis, Martin L. Watzenboeck, Robert Nica, Clement Staud, Lukas Hammerl, Philipp WohlfarthRupert C. Ecker, Sylvia Knapp, Werner Rabitsch, David Berry, Georg Stary^*

^*Kontaktforfatter

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

3 Citationer (Scopus)

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.

Originalsprog	Engelsk
Tidsskrift	Leukemia
Vol/bind	36
Udgave nummer	11
Sider (fra-til)	2705-2714
Antal sider	10
ISSN	0887-6924
DOI	https://doi.org/10.1038/s41375-022-01712-z
Status	Udgivet - nov. 2022
Udgivet eksternt	Ja

Bibliografisk note

Funding Information:
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).

Funding Information:
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).

Publisher Copyright:
© 2022, The Author(s), under exclusive licence to Springer Nature Limited.

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10.1038/s41375-022-01712-z

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Bayer, N., Hausman, B., Pandey, R. V., Deckert, F., Gail, L. M., Strobl, J., Pjevac, P., Krall, C., Unterluggauer, L., Redl, A., Bachmayr, V., Kleissl, L., Nehr, M., Kirkegaard, R., Makristathis, A., Watzenboeck, M. L., Nica, R., Staud, C., Hammerl, L., ... Stary, G. (2022). Disturbances in microbial skin recolonization and cutaneous immune response following allogeneic stem cell transfer. Leukemia, 36(11), 2705-2714. https://doi.org/10.1038/s41375-022-01712-z

@article{c8e0da1948fb430096bae091ec5167fa,

title = "Disturbances in microbial skin recolonization and cutaneous immune response following allogeneic stem cell transfer",

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.",

keywords = "Gastrointestinal Microbiome, Graft vs Host Disease/etiology, Hematopoietic Stem Cell Transplantation/adverse effects, Humans, Immunity",

author = "Nadine Bayer and Bela Hausman and Pandey, {Ram Vinay} and Florian Deckert and Gail, {Laura Marie} and Johanna Strobl and Petra Pjevac and Christoph Krall and Luisa Unterluggauer and Anna Redl and Victoria Bachmayr and Lisa Kleissl and Marion Nehr and Rasmus Kirkegaard and Athanasios Makristathis and Watzenboeck, {Martin L.} and Robert Nica and Clement Staud and Lukas Hammerl and Philipp Wohlfarth and Ecker, {Rupert C.} and Sylvia Knapp and Werner Rabitsch and David Berry and Georg Stary",

note = "Publisher Copyright: {\textcopyright} 2022, The Author(s), under exclusive licence to Springer Nature Limited.",

year = "2022",

month = nov,

doi = "10.1038/s41375-022-01712-z",

language = "English",

volume = "36",

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Bayer, N, Hausman, B, Pandey, RV, Deckert, F, Gail, LM, Strobl, J, Pjevac, P, Krall, C, Unterluggauer, L, Redl, A, Bachmayr, V, Kleissl, L, Nehr, M, Kirkegaard, R, Makristathis, A, Watzenboeck, ML, Nica, R, Staud, C, Hammerl, L, Wohlfarth, P, Ecker, RC, Knapp, S, Rabitsch, W, Berry, D & Stary, G 2022, 'Disturbances in microbial skin recolonization and cutaneous immune response following allogeneic stem cell transfer', Leukemia, bind 36, nr. 11, s. 2705-2714. https://doi.org/10.1038/s41375-022-01712-z

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T1 - Disturbances in microbial skin recolonization and cutaneous immune response following allogeneic stem cell transfer

AU - Bayer, Nadine

AU - Hausman, Bela

AU - Pandey, Ram Vinay

AU - Deckert, Florian

AU - Gail, Laura Marie

AU - Strobl, Johanna

AU - Pjevac, Petra

AU - Krall, Christoph

AU - Unterluggauer, Luisa

AU - Redl, Anna

AU - Bachmayr, Victoria

AU - Kleissl, Lisa

AU - Nehr, Marion

AU - Kirkegaard, Rasmus

AU - Makristathis, Athanasios

AU - Watzenboeck, Martin L.

AU - Nica, Robert

AU - Staud, Clement

AU - Hammerl, Lukas

AU - Wohlfarth, Philipp

AU - Ecker, Rupert C.

AU - Knapp, Sylvia

AU - Rabitsch, Werner

AU - Berry, David

AU - Stary, Georg

PY - 2022/11

Y1 - 2022/11

N2 - 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.

AB - 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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KW - Graft vs Host Disease/etiology

KW - Hematopoietic Stem Cell Transplantation/adverse effects

KW - Humans

KW - Immunity

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

Abstract

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