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Mathematical modeling of ovine footrot in the UK: the effect of Dichelobacter nodosus and Fusobacterium necrophorum on the disease dynamics.

ABSTRACT: Dichelobacter nodosus is a virulent, invasive, anaerobic bacterium that is believed to be the causative agent of ovine footrot, an infectious bacterial disease of sheep that causes lameness. Another anaerobe, Fusobacterium necrophorum, has been intimately linked with the disease occurrence and severity. Here we examine data from a longitudinal study of footrot on one UK farm, including quantitative PCR (qPCR) estimates of bacterial load of D. nodosus and F. necrophorum. The data is at foot level; all feet were monitored for five weeks assessing disease severity (healthy, interdigital dermatitis (ID), or severe footrot (SFR)) and bacterial load (number of bacteria/swab). We investigate the role of D. nodosus and F. necrophorum in the progress of the disease using a continuous-time Markov model with 12 different states characterising the foot. The transition rates between the adjacent states are the (34) model parameters, these are determined using Metropolis Hasting MCMC. Our aim is to determine the predictive relationship between past and future D. nodosus and F. necrophorum load and disease states. We demonstrate a high level of predictive accuracy at the population level for the D. nodosus model, although the dynamics of individual feet is highly stochastic. However, we note that this predictive accuracy at population level is only high in more diseased states for F. necrophorum model. This supports our hypothesis that D. nodosus load and status of the foot work in combination to give rise to severe footrot and lameness, and that D. nodosus load plays the primary role in the initiation and progression of footrot, while F. necrophorum load rather increases disease severity of SFR.

SUBMITTER: Atia J

PROVIDER: S-EPMC5729202 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Mathematical modeling of ovine footrot in the UK: the effect of Dichelobacter nodosus and Fusobacterium necrophorum on the disease dynamics.

Atia Jolene J Monaghan Emma E Kaler Jasmeet J Purdy Kevin K Green Laura L Keeling Matt M

Epidemics 20170412

Dichelobacter nodosus is a virulent, invasive, anaerobic bacterium that is believed to be the causative agent of ovine footrot, an infectious bacterial disease of sheep that causes lameness. Another anaerobe, Fusobacterium necrophorum, has been intimately linked with the disease occurrence and severity. Here we examine data from a longitudinal study of footrot on one UK farm, including quantitative PCR (qPCR) estimates of bacterial load of D. nodosus and F. necrophorum. The data is at foot level ...[more]

PMID: 28461081

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Project description:Footrot is an infectious bacterial disease of sheep that causes lameness. The causal agent is Dichelobacter nodosus. There is debate regarding the role of Fusobacterium necrophorum in disease initiation. This research used an observational longitudinal study of footrot, together with quantitative PCR (qPCR) of bacterial load of D. nodosus and F. necrophorum, to elucidate the roles of each species in the development of disease. All feet of 18 a priori selected sheep were monitored for five weeks assessing disease severity (healthy, interdigital dermatitis (ID) and severe footrot (SFR)) and bacterial load. A multinomial model was used to analyse these data. Key unadjusted results were that D. nodosus was detected more frequently on feet with ID, whereas F. necrophorum was detected more frequently on feet with SFR. In the multinomial model, ID was associated with increasing log10 load of D. nodosus the week of observation (OR=1.28 (95% CI=1.08-1.53)) and the week prior to development of ID (OR=1.20 (95% CI=1.01-1.42). There was no association between log10 load(2) of F. necrophorum and presence of ID (OR=0.99 (95% CI=0.96-1.02))). SFR was associated with increasing log10 load of D. nodosus the week before disease onset (OR=1.42 (95% CI=1.02-1.96)) but not once SFR had occurred. SFR was positively associated with log10 load(2) of F. necrophorum once disease was present (OR=1.06 (95% CI=1.01-1.11)). In summary, there was an increased risk of increasing D. nodosus load the week prior to development of ID and SFR and during an episode of ID. In contrast, F. necrophorum load was not associated with ID before or during an episode, and was only associated with SFR once present. These results contribute to our understanding of the epidemiology of footrot and highlight that D. nodosus load plays the primary role in disease initiation and progression, with F. necrophorum load playing a secondary role. Further studies in more flocks and climates would be useful to confirm these findings. This study identifies that D. nodosus load is highest during ID. This supports previous epidemiological findings, which demonstrate that controlling ID is the most effective management strategy to prevent new cases of ID and SFR.

Project description:UNLABELLED:Footrot is a contagious, debilitating disease of sheep, causing major economic losses in most sheep-producing countries. The causative agent is the Gram-negative anaerobe Dichelobacter nodosus. Depending on the virulence of the infective bacterial strain, clinical signs vary from a mild interdigital dermatitis (benign footrot) to severe underrunning of the horn of the hoof (virulent footrot). The aim of this study was to investigate the genetic relationship between D. nodosus strains of different phenotypic virulences and between isolates from different geographic regions. Genome sequencing was performed on 103 D. nodosus isolates from eight different countries. Comparison of these genome sequences revealed that they were highly conserved, with >95% sequence identity. However, single nucleotide polymorphism analysis of the 31,627 nucleotides that were found to differ in one or more of the 103 sequenced isolates divided them into two distinct clades. Remarkably, this division correlated with known virulent and benign phenotypes, as well as with the single amino acid difference between the AprV2 and AprB2 proteases, which are produced by virulent and benign strains, respectively. This division was irrespective of the geographic origin of the isolates. However, within one of these clades, isolates from different geographic regions generally belonged to separate clusters. In summary, we have shown that D. nodosus has a bimodal population structure that is globally conserved and provide evidence that virulent and benign isolates represent two distinct forms of D. nodosus strains. These data have the potential to improve the diagnosis and targeted control of this economically significant disease. IMPORTANCE:The Gram-negative anaerobic bacterium Dichelobacter nodosus is the causative agent of ovine footrot, a disease of major importance to the worldwide sheep industry. The known D. nodosus virulence factors are its type IV fimbriae and extracellular serine proteases. D. nodosus strains are designated virulent or benign based on the type of disease caused under optimal climatic conditions. These isolates have similar fimbriae but distinct extracellular proteases. To determine the relationship between virulent and benign isolates and the relationship of isolates from different geographical regions, a genomic study that involved the sequencing and subsequent analysis of 103 D. nodosus isolates was undertaken. The results showed that D. nodosus isolates are highly conserved at the genomic level but that they can be divided into two distinct clades that correlate with their disease phenotypes and with a single amino acid substitution in one of the extracellular proteases.

Dataset Information

Mathematical modeling of ovine footrot in the UK: the effect of Dichelobacter nodosus and Fusobacterium necrophorum on the disease dynamics.

Publications

Mathematical modeling of ovine footrot in the UK: the effect of Dichelobacter nodosus and Fusobacterium necrophorum on the disease dynamics.

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