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A comprehensive analysis of gut and skin microbiota in canine atopic dermatitis in Shiba Inu dogs

BACKGROUND: Like its human counterpart, canine atopic dermatitis (cAD) is a chronic relapsing condition; thus, most cAD-affected dogs will require lifelong treatment to maintain an acceptable quality of life. A potential intervention is modulation of the composition of gut microbiota, and in fact, p...

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Autores principales: Thomsen, Mirja, Künstner, Axel, Wohlers, Inken, Olbrich, Michael, Lenfers, Tim, Osumi, Takafumi, Shimazaki, Yotaro, Nishifuji, Koji, Ibrahim, Saleh M., Watson, Adrian, Busch, Hauke, Hirose, Misa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10590023/
https://www.ncbi.nlm.nih.gov/pubmed/37864204
http://dx.doi.org/10.1186/s40168-023-01671-2
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author Thomsen, Mirja
Künstner, Axel
Wohlers, Inken
Olbrich, Michael
Lenfers, Tim
Osumi, Takafumi
Shimazaki, Yotaro
Nishifuji, Koji
Ibrahim, Saleh M.
Watson, Adrian
Busch, Hauke
Hirose, Misa
author_facet Thomsen, Mirja
Künstner, Axel
Wohlers, Inken
Olbrich, Michael
Lenfers, Tim
Osumi, Takafumi
Shimazaki, Yotaro
Nishifuji, Koji
Ibrahim, Saleh M.
Watson, Adrian
Busch, Hauke
Hirose, Misa
author_sort Thomsen, Mirja
collection PubMed
description BACKGROUND: Like its human counterpart, canine atopic dermatitis (cAD) is a chronic relapsing condition; thus, most cAD-affected dogs will require lifelong treatment to maintain an acceptable quality of life. A potential intervention is modulation of the composition of gut microbiota, and in fact, probiotic treatment has been proposed and tried in human atopic dermatitis (AD) patients. Since dogs are currently receiving intensive medical care, this will be the same option for dogs, while evidence of gut dysbiosis in cAD is still missing, although skin microbial profiling in cAD has been conducted in several studies. Therefore, we conducted a comprehensive analysis of both gut and skin microbiota in cAD in one specific cAD-predisposed breed, Shiba Inu. Additionally, we evaluated the impact of commonly used medical management on cAD (Janus kinase; JAK inhibitor, oclacitinib) on the gut and skin microbiota. Furthermore, we genotyped the Shiba Inu dogs according to the mitochondrial DNA haplogroup and assessed its association with the composition of the gut microbiota. RESULTS: Staphylococcus was the most predominant bacterial genus observed in the skin; Escherichia/Shigella and Clostridium sensu stricto were highly abundant in the gut of cAD-affected dogs. In the gut microbiota, Fusobacteria and Megamonas were highly abundant in healthy dogs but significantly reduced in cAD-affected dogs. The abundance of these bacterial taxa was positively correlated with the effect of the treatment and state of the disease. Oclacitinib treatment on cAD-affected dogs shifted the composition of microbiota towards that in healthy dogs, and the latter brought it much closer to healthy microbiota, particularly in the gut. Additionally, even within the same dog breed, the mtDNA haplogroup varied, and there was an association between the mtDNA haplogroup and microbial composition in the gut and skin. CONCLUSIONS: Dysbiosis of both the skin and the gut was observed in cAD in Shiba Inu dogs. Our findings provide a basis for the potential treatment of cAD by manipulating the gut microbiota as well as the skin microbiota. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01671-2.
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spelling pubmed-105900232023-10-22 A comprehensive analysis of gut and skin microbiota in canine atopic dermatitis in Shiba Inu dogs Thomsen, Mirja Künstner, Axel Wohlers, Inken Olbrich, Michael Lenfers, Tim Osumi, Takafumi Shimazaki, Yotaro Nishifuji, Koji Ibrahim, Saleh M. Watson, Adrian Busch, Hauke Hirose, Misa Microbiome Research BACKGROUND: Like its human counterpart, canine atopic dermatitis (cAD) is a chronic relapsing condition; thus, most cAD-affected dogs will require lifelong treatment to maintain an acceptable quality of life. A potential intervention is modulation of the composition of gut microbiota, and in fact, probiotic treatment has been proposed and tried in human atopic dermatitis (AD) patients. Since dogs are currently receiving intensive medical care, this will be the same option for dogs, while evidence of gut dysbiosis in cAD is still missing, although skin microbial profiling in cAD has been conducted in several studies. Therefore, we conducted a comprehensive analysis of both gut and skin microbiota in cAD in one specific cAD-predisposed breed, Shiba Inu. Additionally, we evaluated the impact of commonly used medical management on cAD (Janus kinase; JAK inhibitor, oclacitinib) on the gut and skin microbiota. Furthermore, we genotyped the Shiba Inu dogs according to the mitochondrial DNA haplogroup and assessed its association with the composition of the gut microbiota. RESULTS: Staphylococcus was the most predominant bacterial genus observed in the skin; Escherichia/Shigella and Clostridium sensu stricto were highly abundant in the gut of cAD-affected dogs. In the gut microbiota, Fusobacteria and Megamonas were highly abundant in healthy dogs but significantly reduced in cAD-affected dogs. The abundance of these bacterial taxa was positively correlated with the effect of the treatment and state of the disease. Oclacitinib treatment on cAD-affected dogs shifted the composition of microbiota towards that in healthy dogs, and the latter brought it much closer to healthy microbiota, particularly in the gut. Additionally, even within the same dog breed, the mtDNA haplogroup varied, and there was an association between the mtDNA haplogroup and microbial composition in the gut and skin. CONCLUSIONS: Dysbiosis of both the skin and the gut was observed in cAD in Shiba Inu dogs. Our findings provide a basis for the potential treatment of cAD by manipulating the gut microbiota as well as the skin microbiota. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01671-2. BioMed Central 2023-10-21 /pmc/articles/PMC10590023/ /pubmed/37864204 http://dx.doi.org/10.1186/s40168-023-01671-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Thomsen, Mirja
Künstner, Axel
Wohlers, Inken
Olbrich, Michael
Lenfers, Tim
Osumi, Takafumi
Shimazaki, Yotaro
Nishifuji, Koji
Ibrahim, Saleh M.
Watson, Adrian
Busch, Hauke
Hirose, Misa
A comprehensive analysis of gut and skin microbiota in canine atopic dermatitis in Shiba Inu dogs
title A comprehensive analysis of gut and skin microbiota in canine atopic dermatitis in Shiba Inu dogs
title_full A comprehensive analysis of gut and skin microbiota in canine atopic dermatitis in Shiba Inu dogs
title_fullStr A comprehensive analysis of gut and skin microbiota in canine atopic dermatitis in Shiba Inu dogs
title_full_unstemmed A comprehensive analysis of gut and skin microbiota in canine atopic dermatitis in Shiba Inu dogs
title_short A comprehensive analysis of gut and skin microbiota in canine atopic dermatitis in Shiba Inu dogs
title_sort comprehensive analysis of gut and skin microbiota in canine atopic dermatitis in shiba inu dogs
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10590023/
https://www.ncbi.nlm.nih.gov/pubmed/37864204
http://dx.doi.org/10.1186/s40168-023-01671-2
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