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      Evaluation of the effects of anthelmintic administration on the fecal microbiome of healthy dogs with and without subclinical Giardia spp. and Cryptosporidium canis infections

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          Abstract

          Background

          The gastrointestinal microbiome plays an important role in host health and there is increasing concern regarding the deleterious effects of pharmaceuticals on the fecal microbiome. The effect of anthelmintic therapy on the fecal microbiome in dogs has not yet been evaluated. The purpose of this study was to evaluate the effect of anthelmintic administration on the fecal microbiome of dogs with and without subclinical Giardia species and Cryptosporidium canis infections.

          Methodology/Principal findings

          Part 1: 6 healthy adult research beagles with subclinical giardiasis and cryptosporidiosis were administered a commercially available preparation of febantel combined with pyrantel and praziquantel (FPP) orally daily for three days. Part 2: 19 healthy staff-owned dogs without giardiasis or cryptosporidiosis were divided into a treatment group (n = 9) that was administered fenbendazole orally daily for five days and an untreated control group (n = 10). For both parts of the study, feces were collected at multiple time points before and after anthelmintic (FPP or fenbendazole) administration. Fecal DNA was extracted for Illumina sequencing of the bacterial 16S rRNA gene and qPCR assays. Neither FPP nor fenbendazole treatment caused a significant change in alpha or beta diversity or the relative abundance of bacterial species. Upon univariate statistical analysis neither FPP or fenbendazole caused minimal changes in the fecal microbiota.

          Conclusion

          FPP administration was associated with minimal alterations of the fecal microbiome of healthy research beagles with subclinical giardiasis and cryptosporidiosis. Fenbendazole administration was associated with minimal alterations of the fecal microbiome of healthy staff owned dogs.

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          Most cited references 34

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          UniFrac: a new phylogenetic method for comparing microbial communities.

          We introduce here a new method for computing differences between microbial communities based on phylogenetic information. This method, UniFrac, measures the phylogenetic distance between sets of taxa in a phylogenetic tree as the fraction of the branch length of the tree that leads to descendants from either one environment or the other, but not both. UniFrac can be used to determine whether communities are significantly different, to compare many communities simultaneously using clustering and ordination techniques, and to measure the relative contributions of different factors, such as chemistry and geography, to similarities between samples. We demonstrate the utility of UniFrac by applying it to published 16S rRNA gene libraries from cultured isolates and environmental clones of bacteria in marine sediment, water, and ice. Our results reveal that (i) cultured isolates from ice, water, and sediment resemble each other and environmental clone sequences from sea ice, but not environmental clone sequences from sediment and water; (ii) the geographical location does not correlate strongly with bacterial community differences in ice and sediment from the Arctic and Antarctic; and (iii) bacterial communities differ between terrestrially impacted seawater (whether polar or temperate) and warm oligotrophic seawater, whereas those in individual seawater samples are not more similar to each other than to those in sediment or ice samples. These results illustrate that UniFrac provides a new way of characterizing microbial communities, using the wealth of environmental rRNA sequences, and allows quantitative insight into the factors that underlie the distribution of lineages among environments.
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            The impact of the gut microbiota on human health: an integrative view.

            The human gut harbors diverse microbes that play a fundamental role in the well-being of their host. The constituents of the microbiota--bacteria, viruses, and eukaryotes--have been shown to interact with one another and with the host immune system in ways that influence the development of disease. We review these interactions and suggest that a holistic approach to studying the microbiota that goes beyond characterization of community composition and encompasses dynamic interactions between all components of the microbiota and host tissue over time will be crucial for building predictive models for diagnosis and treatment of diseases linked to imbalances in our microbiota. Copyright © 2012 Elsevier Inc. All rights reserved.
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              The Fecal Microbiome in Dogs with Acute Diarrhea and Idiopathic Inflammatory Bowel Disease

              Background Recent molecular studies have revealed a highly complex bacterial assembly in the canine intestinal tract. There is mounting evidence that microbes play an important role in the pathogenesis of acute and chronic enteropathies of dogs, including idiopathic inflammatory bowel disease (IBD). The aim of this study was to characterize the bacterial microbiota in dogs with various gastrointestinal disorders. Methodology/Principal Findings Fecal samples from healthy dogs (n = 32), dogs with acute non-hemorrhagic diarrhea (NHD; n = 12), dogs with acute hemorrhagic diarrhea (AHD; n = 13), and dogs with active (n = 9) and therapeutically controlled idiopathic IBD (n = 10) were analyzed by 454-pyrosequencing of the 16S rRNA gene and qPCR assays. Dogs with acute diarrhea, especially those with AHD, had the most profound alterations in their microbiome, as significant separations were observed on PCoA plots of unweighted Unifrac distances. Dogs with AHD had significant decreases in Blautia, Ruminococcaceae including Faecalibacterium, and Turicibacter spp., and significant increases in genus Sutterella and Clostridium perfringens when compared to healthy dogs. No significant separation on PCoA plots was observed for the dogs with IBD. Faecalibacterium spp. and Fusobacteria were, however, decreased in the dogs with clinically active IBD, but increased during time periods of clinically insignificant IBD, as defined by a clinical IBD activity index (CIBDAI). Conclusions Results of this study revealed a bacterial dysbiosis in fecal samples of dogs with various GI disorders. The observed changes in the microbiome differed between acute and chronic disease states. The bacterial groups that were commonly decreased during diarrhea are considered to be important short-chain fatty acid producers and may be important for canine intestinal health. Future studies should correlate these observed phylogenetic differences with functional changes in the intestinal microbiome of dogs with defined disease phenotypes.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                6 February 2020
                2020
                : 15
                : 2
                Affiliations
                [1 ] Small Animal Clinical Sciences, Gastrointestinal Laboratory, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, Texas, United States of America
                [2 ] Center for Companion Animal Studies, Colorado State University, Fort Collins, Colorado, United States of America
                University of Illinois, UNITED STATES
                Author notes

                Competing Interests: The authors have read the journal's policy and the authors of this manuscript have the following competing interests to declare: Drs. Lidbury, Steiner and Suchodolski are affiliated with the Gastrointestinal Laboratory, Texas A&M University that offers the Canine Fecal Dysbiosis Index and fecal tests for Clostridium perfringens and Clostridium difficile on a fee-for-service basis. Dr. Lappin has received past research support as well as acted as consultant and a sponsored speaker for Bayer Animal Health. This does not alter our adherence to PLOS ONE policies on sharing data and materials. These funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. There are no patents, products in development or marketed products associated with this research to declare.

                Article
                PONE-D-19-18748
                10.1371/journal.pone.0228145
                7004322
                32027665
                © 2020 Fujishiro et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Counts
                Figures: 9, Tables: 3, Pages: 17
                Product
                Funding
                This study was funded by: Bayer Animal Health ( https://animalhealth.bayer.com/) and the Colorado State University Center for Companion Animal Studies ( http://csu-cvmbs.colostate.edu/vth/veterinarians/research/companion-animals/Pages/default.aspx). This study was also funded by a generous gift from Livingston and Saranne Kosberg. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Dogs
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbiome
                Biology and Life Sciences
                Genetics
                Genomics
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Microbiology
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Giardia
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Giardiasis
                Medicine and Health Sciences
                Parasitic Diseases
                Parasitic Intestinal Diseases
                Giardiasis
                Medicine and Health Sciences
                Parasitic Diseases
                Protozoan Infections
                Giardiasis
                Biology and life sciences
                Molecular biology
                Molecular biology techniques
                Biomolecular isolation
                DNA isolation
                Research and analysis methods
                Molecular biology techniques
                Biomolecular isolation
                DNA isolation
                Biology and life sciences
                Biochemistry
                Nucleic acids
                RNA
                Non-coding RNA
                Ribosomal RNA
                Biology and life sciences
                Biochemistry
                Ribosomes
                Ribosomal RNA
                Biology and life sciences
                Cell biology
                Cellular structures and organelles
                Ribosomes
                Ribosomal RNA
                Medicine and Health Sciences
                Parasitic Diseases
                Cryptosporidiosis
                Biology and Life Sciences
                Organisms
                Bacteria
                Custom metadata
                All relevant data are within the manuscript and its supporting information files. Our next generation sequencing results have been uploaded to a public data repository: NCBI Sequence Read Archive (SRA), the submission numbers are SRP162534 for the FFP study and SRP163138 for the fenbendazole study.

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