{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,28]],"date-time":"2026-10-28T17:36:40Z","timestamp":1793209000460,"version":"4.5.0"},"reference-count":70,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2023,10,21]],"date-time":"2023-10-21T00:00:00Z","timestamp":1697846400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2023,10,21]],"date-time":"2023-10-21T00:00:00Z","timestamp":1697846400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100009525","name":"WALTHAM Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100009525","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004168","name":"Universit\u00e4t zu L\u00fcbeck","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100004168","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Microbiome"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Background<\/jats:title>\n                    <jats:p>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.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      <jats:italic>Staphylococcus<\/jats:italic>\n                      was the most predominant bacterial genus observed in the skin;\n                      <jats:italic>Escherichia\/Shigella<\/jats:italic>\n                      and\n                      <jats:italic>Clostridium sensu stricto<\/jats:italic>\n                      were highly abundant in the gut of cAD-affected dogs. In the gut microbiota,\n                      <jats:italic>Fusobacteria<\/jats:italic>\n                      and\n                      <jats:italic>Megamonas<\/jats:italic>\n                      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.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>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.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1186\/s40168-023-01671-2","type":"journal-article","created":{"date-parts":[[2023,10,20]],"date-time":"2023-10-20T21:02:35Z","timestamp":1697835755000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":36,"title":["A comprehensive analysis of gut and skin microbiota in canine atopic dermatitis in Shiba Inu dogs"],"prefix":"10.1186","volume":"11","author":[{"given":"Mirja","family":"Thomsen","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0692-2105","authenticated-orcid":false,"given":"Axel","family":"K\u00fcnstner","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4004-0464","authenticated-orcid":false,"given":"Inken","family":"Wohlers","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Olbrich","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tim","family":"Lenfers","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takafumi","family":"Osumi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yotaro","family":"Shimazaki","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Koji","family":"Nishifuji","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7827-2290","authenticated-orcid":false,"given":"Saleh M.","family":"Ibrahim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrian","family":"Watson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4763-4521","authenticated-orcid":false,"given":"Hauke","family":"Busch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8909-4693","authenticated-orcid":false,"given":"Misa","family":"Hirose","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,10,21]]},"reference":[{"key":"1671_CR1","doi-asserted-by":"crossref","first-page":"10460","DOI":"10.1038\/ncomms10460","volume":"7","author":"JJ Hayward","year":"2016","unstructured":"Hayward JJ, Castelhano MG, Oliveira KC, Corey E, Balkman C, Baxter TL, et al. Complex disease and phenotype mapping in the domestic dog. Nat Commun. 2016;7:10460.","journal-title":"Nat Commun"},{"key":"1671_CR2","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1038\/s41568-020-0297-3","volume":"20","author":"AK LeBlanc","year":"2020","unstructured":"LeBlanc AK, Mazcko CN. Improving human cancer therapy through the evaluation of pet dogs. Nat Rev Cancer. 2020;20:727\u201342.","journal-title":"Nat Rev Cancer"},{"key":"1671_CR3","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1146\/annurev-animal-051021-080937","volume":"10","author":"A Ruple","year":"2022","unstructured":"Ruple A, MacLean E, Snyder-Mackler N, Creevy KE, Promislow D. Dog models of aging. Annu Rev Anim Biosci. 2022;10:419\u201339.","journal-title":"Annu Rev Anim Biosci"},{"key":"1671_CR4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41572-018-0001-z","volume":"4","author":"S Weidinger","year":"2018","unstructured":"Weidinger S, Beck LA, Bieber T, Kabashima K, Irvine AD. Atopic dermatitis. Nat Rev Dis Primer. 2018;4:1\u201320.","journal-title":"Nat Rev Dis Primer"},{"key":"1671_CR5","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1186\/s13601-018-0228-5","volume":"8","author":"NKY Gedon","year":"2018","unstructured":"Gedon NKY, Mueller RS. Atopic dermatitis in cats and dogs: a difficult disease for animals and owners. Clin Transl Allergy. 2018;8:41.","journal-title":"Clin Transl Allergy"},{"key":"1671_CR6","doi-asserted-by":"crossref","first-page":"1291","DOI":"10.2460\/javma.254.11.1291","volume":"254","author":"TJ Nuttall","year":"2019","unstructured":"Nuttall TJ, Marsella R, Rosenbaum MR, Gonzales AJ, Fadok VA. Update on pathogenesis, diagnosis, and treatment of atopic dermatitis in dogs. J Am Vet Med Assoc. 2019;254:1291\u2013300.","journal-title":"J Am Vet Med Assoc"},{"key":"1671_CR7","doi-asserted-by":"crossref","first-page":"2351","DOI":"10.1038\/jid.2009.98","volume":"129","author":"R Marsella","year":"2009","unstructured":"Marsella R, Girolomoni G. Canine models of atopic dermatitis: a useful tool with untapped potential. J Invest Dermatol. 2009;129:2351\u20137.","journal-title":"J Invest Dermatol"},{"key":"1671_CR8","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1111\/j.1365-3164.2009.00845.x","volume":"21","author":"K Jaeger","year":"2010","unstructured":"Jaeger K, Linek M, Power HT, Bettenay SV, Zabel S, Rosychuk RAW, et al. Breed and site predispositions of dogs with atopic dermatitis: a comparison of five locations in three continents. Vet Dermatol. 2010;21:118\u201322.","journal-title":"Vet Dermatol"},{"key":"1671_CR9","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1007\/s11882-015-0567-4","volume":"15","author":"MR Williams","year":"2015","unstructured":"Williams MR, Gallo RL. The role of the skin microbiome in atopic dermatitis. Curr Allergy Asthma Rep. 2015;15:65.","journal-title":"Curr Allergy Asthma Rep"},{"key":"1671_CR10","first-page":"26191","volume":"26","author":"S Carding","year":"2015","unstructured":"Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis. 2015;26:26191.","journal-title":"Microb Ecol Health Dis"},{"key":"1671_CR11","doi-asserted-by":"crossref","first-page":"850","DOI":"10.1101\/gr.131029.111","volume":"22","author":"HH Kong","year":"2012","unstructured":"Kong HH, Oh J, Deming C, Conlan S, Grice EA, Beatson MA, et al. Temporal shifts in the skin microbiome associated with disease flares and treatment in children with atopic dermatitis. Genome Res. 2012;22:850\u20139.","journal-title":"Genome Res"},{"key":"1671_CR12","doi-asserted-by":"crossref","first-page":"e83197","DOI":"10.1371\/journal.pone.0083197","volume":"9","author":"A Rodrigues Hoffmann","year":"2014","unstructured":"Rodrigues Hoffmann A, Patterson AP, Diesel A, Lawhon SD, Ly HJ, Elkins Stephenson C, et al. The skin microbiome in healthy and allergic dogs. PloS One. 2014;9:e83197.","journal-title":"PloS One"},{"key":"1671_CR13","doi-asserted-by":"crossref","first-page":"1182","DOI":"10.1016\/j.jid.2016.01.023","volume":"136","author":"CW Bradley","year":"2016","unstructured":"Bradley CW, Morris DO, Rankin SC, Cain CL, Misic AM, Houser T, et al. Longitudinal evaluation of the skin microbiome and association with microenvironment and treatment in canine atopic dermatitis. J Invest Dermatol. 2016;136:1182\u201390.","journal-title":"J Invest Dermatol"},{"key":"1671_CR14","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.vetmic.2018.12.022","volume":"229","author":"S Chermprapai","year":"2019","unstructured":"Chermprapai S, Ederveen THA, Broere F, Broens EM, Schlotter YM, van Schalkwijk S, et al. The bacterial and fungal microbiome of the skin of healthy dogs and dogs with atopic dermatitis and the impact of topical antimicrobial therapy, an exploratory study. Vet Microbiol. 2019;229:90\u20139.","journal-title":"Vet Microbiol"},{"key":"1671_CR15","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1111\/j.1365-3164.2009.00745.x","volume":"20","author":"J Fazakerley","year":"2009","unstructured":"Fazakerley J, Nuttall T, Sales D, Schmidt V, Carter SD, Hart CA, et al. Staphylococcal colonization of mucosal and lesional skin sites in atopic and healthy dogs. Vet Dermatol. 2009;20:179\u201384.","journal-title":"Vet Dermatol"},{"key":"1671_CR16","doi-asserted-by":"crossref","first-page":"354","DOI":"10.4168\/aair.2018.10.4.354","volume":"10","author":"SY Lee","year":"2018","unstructured":"Lee SY, Lee E, Park YM, Hong SJ. Microbiome in the gut-skin axis in atopic dermatitis. Allergy Asthma Immunol Res. 2018;10:354\u201362.","journal-title":"Allergy Asthma Immunol Res"},{"key":"1671_CR17","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1002\/bies.201600008","volume":"38","author":"CA O\u2019Neill","year":"2016","unstructured":"O\u2019Neill CA, Monteleone G, McLaughlin JT, Paus R. The gut-skin axis in health and disease: A paradigm with therapeutic implications. BioEssays News Rev Mol Cell Dev Biol. 2016;38:1167\u201376.","journal-title":"BioEssays News Rev Mol Cell Dev Biol"},{"key":"1671_CR18","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1126\/science.1241165","volume":"341","author":"PM Smith","year":"2013","unstructured":"Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science. 2013;341:569\u201373.","journal-title":"Science"},{"key":"1671_CR19","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1016\/j.jid.2016.11.014","volume":"137","author":"A Schwarz","year":"2017","unstructured":"Schwarz A, Bruhs A, Schwarz T. The short-chain fatty acid sodium butyrate functions as a regulator of the skin immune system. J Invest Dermatol. 2017;137:855\u201364.","journal-title":"J Invest Dermatol"},{"key":"1671_CR20","doi-asserted-by":"crossref","unstructured":"Fang Z, Li L, Zhang H, Zhao J, Lu W, Chen W. Gut microbiota, probiotics, and their interactions in prevention and treatment of atopic dermatitis: a review.\u00a0Front Immunol. 2021;12:720393.","DOI":"10.3389\/fimmu.2021.720393"},{"key":"1671_CR21","first-page":"2377","volume":"12","author":"A Rostaher","year":"2022","unstructured":"Rostaher A, Morsy Y, Favrot C, Unterer S, Schnyder M, Scharl M, et al. Comparison of the gut microbiome between atopic and healthy dogs-preliminary data. Anim Open Access J MDPI. 2022;12:2377.","journal-title":"Anim Open Access J MDPI"},{"key":"1671_CR22","doi-asserted-by":"crossref","first-page":"1607","DOI":"10.1111\/lam.13828","volume":"75","author":"J Uchiyama","year":"2022","unstructured":"Uchiyama J, Osumi T, Mizukami K, Fukuyama T, Shima A, Unno A, et al. Characterization of the oral and faecal microbiota associated with atopic dermatitis in dogs selected from a purebred Shiba Inu colony. Lett Appl Microbiol. 2022;75:1607\u201316.","journal-title":"Lett Appl Microbiol"},{"key":"1671_CR23","doi-asserted-by":"crossref","first-page":"8824","DOI":"10.1038\/s41598-023-35565-y","volume":"13","author":"K Sugita","year":"2023","unstructured":"Sugita K, Shima A, Takahashi K, Ishihara G, Kawano K, Ohmori K. Pilot evaluation of a single oral fecal microbiota transplantation for canine atopic dermatitis. Sci Rep. 2023;13:8824.","journal-title":"Sci Rep"},{"key":"1671_CR24","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1292\/jvms.20-0301","volume":"82","author":"K Tanaka","year":"2020","unstructured":"Tanaka K, Yamamoto-Fukuda M, Takizawa T, Shimakura H, Sakaguchi M. Association analysis of non-synonymous polymorphisms of interleukin-4 receptor-\u03b1 and interleukin-13 genes in canine atopic dermatitis. J Vet Med Sci. 2020;82:1253\u20139.","journal-title":"J Vet Med Sci"},{"key":"1671_CR25","doi-asserted-by":"crossref","first-page":"371","DOI":"10.2478\/pjvs-2014-0053","volume":"17","author":"M Fujimura","year":"2014","unstructured":"Fujimura M, Ishimaru H, Nakatsuji Y. Fluoxetine (SSRI) treatment of canine atopic dermatitis: a randomized, double-blind, placebo-controlled, crossover trial. Pol J Vet Sci. 2014;17:371\u20133.","journal-title":"Pol J Vet Sci"},{"key":"1671_CR26","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1007\/s00251-009-0402-y","volume":"61","author":"SH Wood","year":"2009","unstructured":"Wood SH, Ke X, Nuttall T, McEwan N, Ollier WE, Carter SD. Genome-wide association analysis of canine atopic dermatitis and identification of disease related SNPs. Immunogenetics. 2009;61:765\u201372.","journal-title":"Immunogenetics"},{"key":"1671_CR27","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1186\/1471-2164-15-257","volume":"15","author":"J Ma","year":"2014","unstructured":"Ma J, Coarfa C, Qin X, Bonnen PE, Milosavljevic A, Versalovic J, et al. mtDNA haplogroup and single nucleotide polymorphisms structure human microbiome communities. BMC Genomics. 2014;15:257.","journal-title":"BMC Genomics"},{"key":"1671_CR28","doi-asserted-by":"crossref","first-page":"15293","DOI":"10.1038\/s41598-017-15377-7","volume":"7","author":"M Hirose","year":"2017","unstructured":"Hirose M, K\u00fcnstner A, Schilf P, S\u00fcnderhauf A, Rupp J, J\u00f6hren O, et al. Mitochondrial gene polymorphism is associated with gut microbial communities in mice. Sci Rep. 2017;7:15293.","journal-title":"Sci Rep."},{"key":"1671_CR29","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1186\/s12917-015-0515-5","volume":"11","author":"P Hensel","year":"2015","unstructured":"Hensel P, Santoro D, Favrot C, Hill P, Griffin C. Canine atopic dermatitis: detailed guidelines for diagnosis and allergen identification. BMC Vet Res. 2015;11:196.","journal-title":"BMC Vet Res"},{"key":"1671_CR30","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1111\/j.1365-3164.2007.00569.x","volume":"18","author":"T Olivry","year":"2007","unstructured":"Olivry T, Marsella R, Iwasaki T, Mueller R, Dermatitis TITFOCA. Validation of CADESI-03, a severity scale for clinical trials enrolling dogs with atopic dermatitis. Vet Dermatol. 2007;18:78\u201386.","journal-title":"Vet Dermatol"},{"issue":"77\u201385","key":"1671_CR31","first-page":"e25","volume":"25","author":"T Olivry","year":"2014","unstructured":"Olivry T, Saridomichelakis M, Nuttall T, Bensignor E, Griffin CE, Hill PB, et al. Validation of the Canine atopic Dermatitis Extent and Severity Index (CADESI)-4, a simplified severity scale for assessing skin lesions of atopic dermatitis in dogs. Vet Dermatol. 2014;25(77\u201385):e25.","journal-title":"Vet Dermatol"},{"key":"1671_CR32","doi-asserted-by":"crossref","first-page":"2117","DOI":"10.1016\/j.jid.2022.01.020","volume":"142","author":"A Reimer-Taschenbrecker","year":"2022","unstructured":"Reimer-Taschenbrecker A, K\u00fcnstner A, Hirose M, H\u00fcbner S, Gewert S, Ibrahim S, et al. Predominance of staphylococcus correlates with wound burden and disease activity in dystrophic epidermolysis bullosa: a prospective case-control study. J Invest Dermatol. 2022;142:2117-2127.e8.","journal-title":"J Invest Dermatol"},{"key":"1671_CR33","doi-asserted-by":"crossref","first-page":"1056","DOI":"10.3390\/ijms23031056","volume":"23","author":"A K\u00fcnstner","year":"2022","unstructured":"K\u00fcnstner A, Schilf P, Busch H, Ibrahim SM, Hirose M. Changes of gut microbiota by natural mtDNA variant differences augment susceptibility to metabolic disease and ageing. Int J Mol Sci. 2022;23:1056.","journal-title":"Int J Mol Sci"},{"key":"1671_CR34","unstructured":"Human mtDNA Genome For the Illumina Sequencing Platform. Available online at https:\/\/emea.support.illumina.com\/content\/dam\/illumina-support\/documents\/documentation\/chemistry_documentation\/samplepreps_legacy\/human-mtdna-genome-guide-15037958-01.pdf. Accessed 21 Sep 2023."},{"key":"1671_CR35","doi-asserted-by":"crossref","first-page":"e2584","DOI":"10.7717\/peerj.2584","volume":"4","author":"T Rognes","year":"2016","unstructured":"Rognes T, Flouri T, Nichols B, Quince C, Mah\u00e9 F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584.","journal-title":"PeerJ"},{"key":"1671_CR36","doi-asserted-by":"crossref","first-page":"996","DOI":"10.1038\/nmeth.2604","volume":"10","author":"RC Edgar","year":"2013","unstructured":"Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996\u20138.","journal-title":"Nat Methods"},{"key":"1671_CR37","doi-asserted-by":"publisher","unstructured":"Edgar RC. SINTAX: a simple non-Bayesian taxonomy classifier for 16S and ITS sequences. bioRxiv. 2016. https:\/\/doi.org\/10.1101\/074161.","DOI":"10.1101\/074161"},{"key":"1671_CR38","doi-asserted-by":"crossref","first-page":"D633","DOI":"10.1093\/nar\/gkt1244","volume":"42 Database iss","author":"JR Cole","year":"2014","unstructured":"Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 2014;42 Database issue:D633-642.","journal-title":"Nucleic Acids Res."},{"key":"1671_CR39","doi-asserted-by":"crossref","first-page":"7537","DOI":"10.1128\/AEM.01541-09","volume":"75","author":"PD Schloss","year":"2009","unstructured":"Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009;75:7537\u201341.","journal-title":"Appl Environ Microbiol"},{"key":"1671_CR40","doi-asserted-by":"crossref","first-page":"D590","DOI":"10.1093\/nar\/gks1219","volume":"41","author":"C Quast","year":"2013","unstructured":"Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590-6.","journal-title":"Nucleic Acids Res"},{"key":"1671_CR41","doi-asserted-by":"crossref","first-page":"e61217","DOI":"10.1371\/journal.pone.0061217","volume":"8","author":"PJ McMurdie","year":"2013","unstructured":"McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PloS One. 2013;8:e61217.","journal-title":"PloS One"},{"key":"1671_CR42","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1186\/s40168-018-0605-2","volume":"6","author":"NM Davis","year":"2018","unstructured":"Davis NM, Proctor DM, Holmes SP, Relman DA, Callahan BJ. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome. 2018;6:226.","journal-title":"Microbiome"},{"key":"1671_CR43","doi-asserted-by":"publisher","unstructured":"Willis AD, Martin BD. Estimating diversity in networked ecological communities. Biostatistics. 2020. https:\/\/doi.org\/10.1093\/biostatistics\/kxaa015.","DOI":"10.1093\/biostatistics\/kxaa015"},{"key":"1671_CR44","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1111\/rssc.12206","volume":"66","author":"A Willis","year":"2017","unstructured":"Willis A, Bunge J, Whitman T. Improved detection of changes in species richness in high diversity microbial communities. J R Stat Soc Ser C Appl Stat. 2017;66:963\u201377.","journal-title":"J R Stat Soc Ser C Appl Stat"},{"key":"1671_CR45","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1111\/j.2517-6161.1982.tb01195.x","volume":"44","author":"J Aitchison","year":"1982","unstructured":"Aitchison J. The statistical analysis of compositional data. J R Stat Soc Ser B Methodol. 1982;44:139\u201377.","journal-title":"J R Stat Soc Ser B Methodol"},{"key":"1671_CR46","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1214\/19-AOAS1283","volume":"14","author":"BD Martin","year":"2020","unstructured":"Martin BD, Witten D, Willis AD. Modeling microbial abundances and dysbiosis with beta-binomial regression. Ann Appl Stat. 2020;14:94\u2013115.","journal-title":"Ann Appl Stat"},{"key":"1671_CR47","doi-asserted-by":"crossref","first-page":"3514","DOI":"10.1038\/s41467-020-17041-7","volume":"11","author":"H Lin","year":"2020","unstructured":"Lin H, Peddada SD. Analysis of compositions of microbiomes with bias correction. Nat Commun. 2020;11:3514.","journal-title":"Nat Commun"},{"key":"1671_CR48","doi-asserted-by":"crossref","first-page":"lqaa029","DOI":"10.1093\/nargab\/lqaa029","volume":"2","author":"A Susin","year":"2020","unstructured":"Susin A, Wang Y, L\u00ea Cao K-A, Calle ML. Variable selection in microbiome compositional data analysis. NAR Genomics Bioinforma. 2020;2:lqaa029.","journal-title":"NAR Genomics Bioinforma"},{"key":"1671_CR49","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1093\/bioinformatics\/btp324","volume":"25","author":"H Li","year":"2009","unstructured":"Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinforma Oxf Engl. 2009;25:1754\u201360.","journal-title":"Bioinforma Oxf Engl."},{"key":"1671_CR50","doi-asserted-by":"crossref","first-page":"giab008","DOI":"10.1093\/gigascience\/giab008","volume":"10","author":"P Danecek","year":"2021","unstructured":"Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, et al. Twelve years of SAMtools and BCFtools. GigaScience. 2021;10:giab008.","journal-title":"GigaScience"},{"key":"1671_CR51","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1186\/s12863-017-0528-0","volume":"18","author":"QK Thai","year":"2017","unstructured":"Thai QK, Chung DA, Tran H-D. Canis mtDNA HV1 database: a web-based tool for collecting and surveying Canis mtDNA HV1 haplotype in public database. BMC Genet. 2017;18:60.","journal-title":"BMC Genet"},{"key":"1671_CR52","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1111\/j.1574-6941.2008.00521.x","volume":"66","author":"JS Suchodolski","year":"2008","unstructured":"Suchodolski JS, Camacho J, Steiner JM. Analysis of bacterial diversity in the canine duodenum, jejunum, ileum, and colon by comparative 16S rRNA gene analysis. FEMS Microbiol Ecol. 2008;66:567\u201378.","journal-title":"FEMS Microbiol Ecol"},{"key":"1671_CR53","doi-asserted-by":"crossref","first-page":"832","DOI":"10.1038\/ismej.2014.179","volume":"9","author":"M Vital","year":"2015","unstructured":"Vital M, Gao J, Rizzo M, Harrison T, Tiedje JM. Diet is a major factor governing the fecal butyrate-producing community structure across Mammalia Aves and Reptilia. ISME J. 2015;9:832\u201343.","journal-title":"ISME J"},{"key":"1671_CR54","doi-asserted-by":"crossref","first-page":"1971","DOI":"10.1002\/ibd.21606","volume":"17","author":"J Strauss","year":"2011","unstructured":"Strauss J, Kaplan GG, Beck PL, Rioux K, Panaccione R, Devinney R, et al. Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm Bowel Dis. 2011;17:1971\u20138.","journal-title":"Inflamm Bowel Dis"},{"key":"1671_CR55","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1046\/j.1440-1746.2002.02834.x","volume":"17","author":"T Ohkusa","year":"2002","unstructured":"Ohkusa T, Sato N, Ogihara T, Morita K, Ogawa M, Okayasu I. Fusobacterium varium localized in the colonic mucosa of patients with ulcerative colitis stimulates species-specific antibody. J Gastroenterol Hepatol. 2002;17:849\u201353.","journal-title":"J Gastroenterol Hepatol"},{"key":"1671_CR56","doi-asserted-by":"crossref","first-page":"1443","DOI":"10.1126\/science.aal5240","volume":"358","author":"S Bullman","year":"2017","unstructured":"Bullman S, Pedamallu CS, Sicinska E, Clancy TE, Zhang X, Cai D, et al. Analysis of Fusobacterium persistence and antibiotic response in colorectal cancer. Science. 2017;358:1443\u20138.","journal-title":"Science"},{"key":"1671_CR57","doi-asserted-by":"crossref","first-page":"16177","DOI":"10.1038\/nmicrobiol.2016.177","volume":"1","author":"Y V\u00e1zquez-Baeza","year":"2016","unstructured":"V\u00e1zquez-Baeza Y, Hyde ER, Suchodolski JS, Knight R. Dog and human inflammatory bowel disease rely on overlapping yet distinct dysbiosis networks. Nat Microbiol. 2016;1:16177.","journal-title":"Nat Microbiol"},{"key":"1671_CR58","doi-asserted-by":"crossref","first-page":"e39333","DOI":"10.1371\/journal.pone.0039333","volume":"7","author":"JS Suchodolski","year":"2012","unstructured":"Suchodolski JS, Dowd SE, Wilke V, Steiner JM, Jergens AE. 16S rRNA gene pyrosequencing reveals bacterial dysbiosis in the duodenum of dogs with idiopathic inflammatory bowel disease. PloS One. 2012;7:e39333.","journal-title":"PloS One"},{"key":"1671_CR59","doi-asserted-by":"crossref","first-page":"1608","DOI":"10.1111\/jvim.15520","volume":"33","author":"Y Minamoto","year":"2019","unstructured":"Minamoto Y, Minamoto T, Isaiah A, Sattasathuchana P, Buono A, Rangachari VR, et al. Fecal short-chain fatty acid concentrations and dysbiosis in dogs with chronic enteropathy. J Vet Intern Med. 2019;33:1608\u201318.","journal-title":"J Vet Intern Med"},{"key":"1671_CR60","doi-asserted-by":"crossref","first-page":"2921","DOI":"10.1099\/ijs.0.2008\/001297-0","volume":"58 Pt 12","author":"R Chevrot","year":"2008","unstructured":"Chevrot R, Carlotti A, Sopena V, Marchand P, Rosenfeld E. Megamonas rupellensis sp. nov., an anaerobe isolated from the caecum of a duck. Int J Syst Evol Microbiol. 2008;58 Pt 12:2921\u20134.","journal-title":"Int J Syst Evol Microbiol"},{"key":"1671_CR61","doi-asserted-by":"crossref","first-page":"970","DOI":"10.1099\/ijs.0.65456-0","volume":"58 Pt 4","author":"H Sakon","year":"2008","unstructured":"Sakon H, Nagai F, Morotomi M, Tanaka R. Sutterella parvirubra sp. Nov. and Megamonas funiformis sp. nov., isolated from human faeces. Int J Syst Evol Microbiol. 2008;58 Pt 4:970\u20135.","journal-title":"Int J Syst Evol Microbiol"},{"key":"1671_CR62","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.1016\/j.jaad.2020.05.130","volume":"83","author":"H Lee","year":"2020","unstructured":"Lee H, Lee JH, Koh S-J, Park H. Bidirectional relationship between atopic dermatitis and inflammatory bowel disease: a systematic review and meta-analysis. J Am Acad Dermatol. 2020;83:1385\u201394.","journal-title":"J Am Acad Dermatol"},{"key":"1671_CR63","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1159\/000505290","volume":"236","author":"X Shi","year":"2020","unstructured":"Shi X, Chen Q, Wang F. The bidirectional association between inflammatory bowel disease and atopic dermatitis: a systematic review and meta-analysis. Dermatol Basel Switz. 2020;236:546\u201353.","journal-title":"Dermatol Basel Switz"},{"key":"1671_CR64","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1016\/j.jaci.2013.05.043","volume":"132","author":"J Penders","year":"2013","unstructured":"Penders J, Gerhold K, Stobberingh EE, Thijs C, Zimmermann K, Lau S, et al. Establishment of the intestinal microbiota and its role for atopic dermatitis in early childhood. J Allergy Clin Immunol. 2013;132:601-607.e8.","journal-title":"J Allergy Clin Immunol"},{"key":"1671_CR65","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1128\/iai.6.3.308-315.1972","volume":"6","author":"DJ Brenner","year":"1972","unstructured":"Brenner DJ, Fanning GR, Steigerwalt AG, Orskov I, Orskov F. Polynucleotide sequence relatedness among three groups of pathogenic Escherichia coli strains. Infect Immun. 1972;6:308\u201315.","journal-title":"Infect Immun"},{"key":"1671_CR66","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.nmni.2017.09.003","volume":"21","author":"NK Devanga Ragupathi","year":"2018","unstructured":"Devanga Ragupathi NK, Muthuirulandi Sethuvel DP, Inbanathan FY, Veeraraghavan B. Accurate differentiation of Escherichia coli and Shigella serogroups: challenges and strategies. New Microbes New Infect. 2018;21:58\u201362.","journal-title":"New Microbes New Infect"},{"key":"1671_CR67","doi-asserted-by":"crossref","first-page":"e9964","DOI":"10.1371\/journal.pone.0009964","volume":"5","author":"P-Y Hong","year":"2010","unstructured":"Hong P-Y, Lee BW, Aw M, Shek LPC, Yap GC, Chua KY, et al. Comparative analysis of fecal microbiota in infants with and without eczema. PloS One. 2010;5:e9964.","journal-title":"PloS One"},{"key":"1671_CR68","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1136\/gut.2006.100164","volume":"56","author":"J Penders","year":"2007","unstructured":"Penders J, Thijs C, van den Brandt PA, Kummeling I, Snijders B, Stelma F, et al. Gut microbiota composition and development of atopic manifestations in infancy: the KOALA Birth Cohort Study. Gut. 2007;56:661\u20137.","journal-title":"Gut"},{"key":"1671_CR69","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1186\/s13040-021-00270-x","volume":"14","author":"S Lewis","year":"2021","unstructured":"Lewis S, Nash A, Li Q, Ahn T-H. Comparison of 16S and whole genome dog microbiomes using machine learning. BioData Min. 2021;14:41.","journal-title":"BioData Min"},{"key":"1671_CR70","doi-asserted-by":"crossref","first-page":"756","DOI":"10.1093\/mmy\/myz118","volume":"58","author":"C Meason-Smith","year":"2020","unstructured":"Meason-Smith C, Olivry T, Lawhon SD, Hoffmann AR. Malassezia species dysbiosis in natural and allergen-induced atopic dermatitis in dogs. Med Mycol. 2020;58:756\u201365.","journal-title":"Med Mycol"}],"container-title":["Microbiome"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s40168-023-01671-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s40168-023-01671-2\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s40168-023-01671-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,31]],"date-time":"2024-10-31T11:01:32Z","timestamp":1730372492000},"score":1,"resource":{"primary":{"URL":"https:\/\/microbiomejournal.biomedcentral.com\/articles\/10.1186\/s40168-023-01671-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,21]]},"references-count":70,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,12]]}},"alternative-id":["1671"],"URL":"https:\/\/doi.org\/10.1186\/s40168-023-01671-2","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2022.07.11.497949","asserted-by":"object"}]},"ISSN":["2049-2618"],"issn-type":[{"value":"2049-2618","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,10,21]]},"assertion":[{"value":"11 July 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 September 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 October 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The Clinical Animal Trials and Research Ethics Committee of the Tokyo University of Agriculture and Technology approved all studies (approval no. 0016021). All participating dog owners were provided with information about the study and gave their written consent before their dogs were included.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"All authors have reviewed the manuscript.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"AW is an employee of Royal Canin SAS, Mars Petcare and that the WALTHAM Foundation is funded by Mars Petcare.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"232"}}