The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis

Abstract Background Contagious Ovine Digital Dermatitis (CODD) is an emerging and common infectious foot disease of sheep which causes severe welfare and economic problems for the sheep industry. The aetiology of the disease is not fully understood and control of the disease is problematic. The aim...

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Main Authors: J. S. Duncan, J. W. Angell, P. Richards, L. Lenzi, G. J. Staton, D. Grove-White, S. Clegg, G. Oikonomou, S. D. Carter, N. J. Evans
Format: Article
Language:English
Published: BMC 2021-02-01
Series:Animal Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s42523-021-00078-4
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author J. S. Duncan
J. W. Angell
P. Richards
L. Lenzi
G. J. Staton
D. Grove-White
S. Clegg
G. Oikonomou
S. D. Carter
N. J. Evans
author_facet J. S. Duncan
J. W. Angell
P. Richards
L. Lenzi
G. J. Staton
D. Grove-White
S. Clegg
G. Oikonomou
S. D. Carter
N. J. Evans
author_sort J. S. Duncan
collection DOAJ
description Abstract Background Contagious Ovine Digital Dermatitis (CODD) is an emerging and common infectious foot disease of sheep which causes severe welfare and economic problems for the sheep industry. The aetiology of the disease is not fully understood and control of the disease is problematic. The aim of this study was to investigate the polybacterial aetiopathogenesis of CODD and the effects of antibiotic treatment, in a longitudinal study of an experimentally induced disease outbreak using a 16S rRNA gene amplicon sequencing approach. Results CODD was induced in 15/30 experimental sheep. During the development of CODD three distinct phenotypic lesion stages were observed. These were an initial interdigital dermatitis (ID) lesion, followed by a footrot (FR) lesion, then finally a CODD lesion. Distinct microbiota were observed for each lesion in terms of microbial diversity, clustering and composition. Porphyromonadaceae, Family XI, Veillonellaceae and Fusobacteriaceae were significantly associated with the diseased feet. Veillonellaceae and Fusobacteriaceae were most associated with the earlier stages of ID and footrot rather than CODD. Following antibiotic treatment of the sheep, the foot microbiota showed a strong tendency to return to the composition of the healthy state. The microbiota composition of CODD lesions collected by swab and biopsy methods were different. In particular, the Spirochaetaceae family were more abundant in samples collected by the biopsy method, suggesting that these bacteria are present in deeper tissues of the diseased foot. Conclusion In this study, CODD presented as part of a spectrum of poly-bacterial foot disease strongly associated with bacterial families Porphyromonadaceae, Family XI (a family in Clostridiales also known as Clostridium cluster XI), Veillonellaceae and Fusobacteriaceae which are predominately Gram-negative anaerobes. Following antibiotic treatment, the microbiome showed a strong tendency to return to the composition of the healthy state. The composition of the healthy foot microbiome does not influence susceptibility to CODD. Based on the data presented here and that CODD appears to be the severest end stage of sheep infectious foot disease lesions, better control of the initial ID and FR lesions would enable better control of CODD and enable better animal welfare.
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spelling doaj.art-ed6cadfa3e9447d1a3bd38b296e6dfb52022-12-21T23:06:11ZengBMCAnimal Microbiome2524-46712021-02-013112110.1186/s42523-021-00078-4The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitisJ. S. Duncan0J. W. Angell1P. Richards2L. Lenzi3G. J. Staton4D. Grove-White5S. Clegg6G. Oikonomou7S. D. Carter8N. J. Evans9Department of Livestock and One Health, Institute of Infection, Veterinary and Ecological Science, University of Liverpool, Leahurst CampusWern Veterinary Surgeons, Department of Research and Innovation, Unit 11Department of Veterinary Pathology, Institute of Infection, Veterinary and Ecological Science, University of Liverpool, Leahurst CampusCentre for Genomic Research, Department of Evolution, Ecology and Behaviour, Institute of Infection, Veterinary and Ecological Science, University of LiverpoolDepartment of Infection Biology & Microbiomes, Institute of Infection, Veterinary and Ecological Science, The University of Liverpool, Leahurst CampusDepartment of Livestock and One Health, Institute of Infection, Veterinary and Ecological Science, University of Liverpool, Leahurst CampusSchool of Life Sciences, College of Science, University of Lincoln, Brayford Pool CampusDepartment of Livestock and One Health, Institute of Infection, Veterinary and Ecological Science, University of Liverpool, Leahurst CampusDepartment of Infection Biology & Microbiomes, Institute of Infection, Veterinary and Ecological Science, The University of Liverpool, Leahurst CampusDepartment of Infection Biology & Microbiomes, Institute of Infection, Veterinary and Ecological Science, The University of Liverpool, Leahurst CampusAbstract Background Contagious Ovine Digital Dermatitis (CODD) is an emerging and common infectious foot disease of sheep which causes severe welfare and economic problems for the sheep industry. The aetiology of the disease is not fully understood and control of the disease is problematic. The aim of this study was to investigate the polybacterial aetiopathogenesis of CODD and the effects of antibiotic treatment, in a longitudinal study of an experimentally induced disease outbreak using a 16S rRNA gene amplicon sequencing approach. Results CODD was induced in 15/30 experimental sheep. During the development of CODD three distinct phenotypic lesion stages were observed. These were an initial interdigital dermatitis (ID) lesion, followed by a footrot (FR) lesion, then finally a CODD lesion. Distinct microbiota were observed for each lesion in terms of microbial diversity, clustering and composition. Porphyromonadaceae, Family XI, Veillonellaceae and Fusobacteriaceae were significantly associated with the diseased feet. Veillonellaceae and Fusobacteriaceae were most associated with the earlier stages of ID and footrot rather than CODD. Following antibiotic treatment of the sheep, the foot microbiota showed a strong tendency to return to the composition of the healthy state. The microbiota composition of CODD lesions collected by swab and biopsy methods were different. In particular, the Spirochaetaceae family were more abundant in samples collected by the biopsy method, suggesting that these bacteria are present in deeper tissues of the diseased foot. Conclusion In this study, CODD presented as part of a spectrum of poly-bacterial foot disease strongly associated with bacterial families Porphyromonadaceae, Family XI (a family in Clostridiales also known as Clostridium cluster XI), Veillonellaceae and Fusobacteriaceae which are predominately Gram-negative anaerobes. Following antibiotic treatment, the microbiome showed a strong tendency to return to the composition of the healthy state. The composition of the healthy foot microbiome does not influence susceptibility to CODD. Based on the data presented here and that CODD appears to be the severest end stage of sheep infectious foot disease lesions, better control of the initial ID and FR lesions would enable better control of CODD and enable better animal welfare.https://doi.org/10.1186/s42523-021-00078-4SheepLamenessCODDFootrotMicrobiome
spellingShingle J. S. Duncan
J. W. Angell
P. Richards
L. Lenzi
G. J. Staton
D. Grove-White
S. Clegg
G. Oikonomou
S. D. Carter
N. J. Evans
The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis
Animal Microbiome
Sheep
Lameness
CODD
Footrot
Microbiome
title The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis
title_full The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis
title_fullStr The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis
title_full_unstemmed The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis
title_short The dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis
title_sort dysbiosis of ovine foot microbiome during the development and treatment of contagious ovine digital dermatitis
topic Sheep
Lameness
CODD
Footrot
Microbiome
url https://doi.org/10.1186/s42523-021-00078-4
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