Contagious ovine digital dermatitis (CODD) is an infectious foot disease of sheep causing severe lameness. Diagnosis is currently made using broad anecdotal descriptions. The aim of this study was to systematically and formally describe the clinical presentation of the disease in terms of (1) a lesion grading system; (2) associated radiographic changes and (3) severity of associated lameness. A five-point lesion grading system was developed and applied to 908 sheep affected by CODD from six farms. Sheep with lesions typical of each grade were euthanased and their feet radiographed. Radiographic abnormalities including soft tissue and bony changes were evident in feet with lesions graded 2–5. In order to quantify the welfare impact of CODD, all the 908 sheep were locomotion scored. Five hundred and eighty-five (64.5% (95% CI 61.4% to 67.6%)) were lame. The locomotion score for affected sheep increased with worsening pathological changes. Once healing had begun the locomotion score decreased. In conclusion the five-point grading system may be used to clinically describe stages of CODD lesions. The radiographic changes revealed examples of deeper pathological changes and there was a strong association between the lesion grading system and locomotion score in affected sheep.
- Contagious ovine digital dermatitis
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Contagious ovine digital dermatitis (CODD) is a relatively new cause of lameness in sheep in the UK, (Harwood and others 1997). Recent surveys of sheep farmers have revealed that CODD has now become common, with farmer reported prevalence of 35 per cent (Angell and others 2014) and 53 per cent (Kaler and Green 2008) identified, and whilst on most affected farms the on-farm prevalence of affected sheep is 2.0 per cent, it can be as much as 50 per cent (Angell and others 2014).
The study of any disease requires a clear case definition to enable diagnosis and monitoring for clinical and research purposes. Currently, CODD is poorly defined in terms of its clinical presentation and the severity of associated lameness. At present, the clinical description of the disease (which is used as the basis of veterinary diagnosis) is limited to anecdotal, broad descriptions of typical foot lesions (Winter 2004, Sargison 2008). Visual inspection of foot lesions is an accepted method of diagnosis for other foot conditions in sheep (Egerton 1989, Foddai and others 2012), and clinical descriptions of the lesions are aided by lesion scoring systems in order to describe specific features in more detail. Currently, there is no standard clinical lesion scoring system for CODD.
Treponemes have been demonstrated in CODD lesions and have been associated with disease (Dhawi and others 2005). In other treponemal associated diseases tissue damage may be extensive and in some cases has had bony involvement, for example in cases of periodontal disease in human beings and toe necrosis in cattle, (Kofler 1999, Loesche and Grossman 2001, Evans and others 2011, Blowey and others 2013). Scott (2010) reported a case series of CODD-like lesions in a group of 10 Cheviot ewes, and using radiography demonstrated osteopenia and resorption/remodelling of the third phalanx of affected digits in some of these sheep.
Sheep with CODD have been observed to be severely lame (Davies and others 1999, Phythian and others 2013), however systematic locomotion scoring, and therefore the implied welfare impact on affected sheep at different stages of disease, has yet to be described.
Therefore, the aim of this paper is to describe the clinical features of CODD in terms of (1) a lesion grading system (2) associated radiographic changes and (3) the severity of associated lameness.
Materials and methods
The study protocol was approved by The University of Liverpool ethics committee (VREC 13) on August 24, 2011.
Development of lesion grading system
Current published clinical descriptions were initially used to establish a case definition of CODD as distinct from other foot conditions, in particular footrot.
CODD was described as an ulcerative or chronic inflammatory lesion at the coronary band, which may extend dorsally and abaxially under the hoof wall and in many cases leads to avulsion of the hoof capsule. The affected digit may be swollen and shortened (Winter 2004, Scott 2010).
Footrot was described as an erythematous and/or an erosive or ulcerative lesion affecting the interdigital space leading to hoof horn separation axially which may lead to necrosis of the sole and in very severe cases lead to avulsion of the hoof capsule (Winter 2004, Sargison 2008).
The definition for CODD was then further developed using previous clinical experience of the authors, together with examination of a photographic archive of CODD lesions to produce the following five-point lesion grading system:
Grade 1 Erosion/ulceration with or without alopecia specifically at the level of the dorsal coronary band.
Grade 2 Erosion/ulceration of the skin at the coronary band with partial (<50 per cent) underrunning of the hoof horn dorsally, abaxially and tending towards circumferential underrunning.
Grade 3 Erosion/ulceration of the skin at the coronary band with 50–100 per cent underrunning of the hoof horn with possible hoof horn avulsion.
Grade 4 Healing foot with the horn beginning to regrow but an active lesion still present.
Grade 5 Healed foot, often with deformation of the regrown horn.
Subsequently, this lesion grading system was applied in the examination of sheep on six farms diagnosed with CODD (Table 1). Over a one-year period each flock was repeatedly inspected between three and six times. At each visit all the sheep in the flocks were inspected closely in the handling pens. All lame sheep were then restrained in dorsal recumbency for detailed examination of their feet. Together with this, depending on feasibility and practical constraints, up to half of the remaining non-lame sheep were also examined in detail. This strategy identified 908 sheep (from 5498 examined) with foot lesions consistent with CODD. The proposed lesion grading system was then used to categorise (by JWA) the 908 sheep affected by CODD in this study and further subtle details and variations within each grade were gathered as a result and used to add detail to the final five-point lesion grading system.
Sheep with lesions typical of the five grades were identified and, with the farmers consent, were euthanased on the farms using pentobarbital sodium (Pentoject; Animal Care). At postmortem, their feet were immediately removed by disarticulation of the radiocarpal or tibiotarsal joints and after gentle washing with a stream of cold water to remove gross contamination were placed immediately in 10 per cent formalin (GCC Diagnostics). This was necessary as the feet were intended to undergo further gross and histopathological examination.
Locomotion scoring sheep affected by CODD
The CODD lesion grade of each of the 908 sheep diagnosed with CODD was recorded. In addition, the gait of all the sheep was observed (before clinical examination) whilst standing and walking to determine their locomotion score using a four-point ordinal locomotion scoring system (Angell and others).
Score 0 (SOUND) Bears weight evenly on all four feet and walks with an even rhythm.
Score 1 (MILDLY LAME) Steps are uneven but it is not clear which limb or limbs are affected.
Score 2 (MODERATELY LAME) Steps are uneven and the stride may be shortened; the affected limb or limbs are identifiable.
Score 3 (SEVERELY LAME) Mobility is severely compromised such that the sheep frequently stops walking or lies down due to obvious discomfort. The affected limb or limbs are clearly identifiable and may be held off the ground whilst walking or standing.
This scoring system was shown to have high levels of intraobserver repeatability when tested by 10 veterinary surgeons (κW 0.81) (Angell and others).
Data were entered into a Microsoft Access database (Microsoft, USA). Graphs and descriptive statistics were performed using STATA IC V.13 (Statacorp, Texas, USA). Median data are presented for the locomotion scoring due to the ordinal nature of the locomotion-scoring tool.
Of the 908 sheep with CODD, 866 (95.4% (95% CI 94.0% to 96.7%)) had CODD in one foot, 42 (4.6% (95% CI 3.3% to 6.0%)) had CODD present in more than one foot. The clinical grading system was used for all 908 sheep and lesions were readily classified using the system. The number of sheep with each grade was not uniform with grades 2 and 5 most commonly represented and grade 1 least represented (6.9% (95% CI 5.3% to 8.6%)) (Table 2).
Lesion grading system
Summary observations and photographs of CODD lesions from using the descriptors in this study include the following:
These lesions were focally extensive, erosive or ulcerative affecting the digital skin and coronary band (Figs 1 and 2). They could be raised (proliferative) or depressed (erosive/ulcerative) and could be reddened or yellow-white (purulent) in colour. At this stage there was no underrunning of the hoof capsule.
The separation occurred between the hoof capsule and the lamellae (Figs 3 and 4). The underrunning varied from the separation of a narrow section of the dorsal hoof wall, to up to 50 per cent of the dorsal and abaxial hoof wall. These digits appeared swollen and grossly the surface of the lamellae appeared rounded and in many cases non-existent. The surface could appear dark red (haemorrhagic) and there was often purulent material adherent to the surface, together with a foul smell.
Up to 100 per cent of the hoof capsule was absent (Figs 7 and 8). Affected digits appeared swollen and the subcorneal tissue exposed by the loss of the hoof wall appeared roughened, dark red (haemorrhagic/necrotic) and friable and could be easily traumatised leading to further bleeding. Often there was obvious shortening of the digit.
Horn regrowth was apparent (Figs 9 and 10). The surface was usually smooth but distorted by circumferential ridges or creases. The affected digit was usually still wider and shortened in comparison to the unaffected digit.
Two digits of each grade, from two different feet in each case were radiographed (Figs 11⇓⇓⇓–15). Lateromedial views are presented as examples only. Key features to note are the extent and appearance of the hoof structures in relation to the bony structures underneath. Demarcation of the laminae is not possible as the hoof horn and laminae are of similar radiodensity.
The locomotion scores of sheep affected by CODD
The locomotion score for affected sheep increased with the grade of CODD, corresponding with a greater degree of underrunning of the hoof horn (Table 2 and Fig 16). Once the hoof capsule had been shed and healing had begun (grade 4) the locomotion score for affected sheep decreased, although sheep with a healed lesion (grade 5) were sometimes still lame. Sheep with more than one foot affected demonstrated a median locomotion score of 2 (IQR 1–2 (range 0–3)). Sheep with all grades of CODD could demonstrate sound gait or severe lameness, and overall, of the 908 sheep with CODD, 585 (64.5% (95% CI 61.4% to 67.6%)) were classified as being lame.
This paper provides a thorough, systematic and detailed description of the clinical and radiographic presentations of CODD. It documents the range of disease presentation observed on six farms over one year and a grading system is proposed by which veterinary practitioners and researchers may describe the clinical signs more consistently. It also provides some radiographic evidence of the changes in feet with CODD at each grade, and using locomotion scoring quantifies the welfare impact to sheep that this disease causes.
Clinical description and grading system
Early in the identification of CODD there was some confusion as to the demarcation of CODD from other differentials (Davies and others 1999, Lewis 1999) in particular footrot. Footrot starts as inflammation of the interdigital skin and may progress axially to underrunning of the hoof horn medially and in extreme cases lead to shedding of the hoof horn capsule (Winter 2004, 2008). It is also possible to observe mixed infections with lesions showing characteristics of both CODD and footrot in some feet (Duncan and others 2012), making diagnosis difficult. Anecdotally there has also been some confusion with cases of Strawberry Footrot, foot abscesses and joint infections. Due to this, careful diagnostic evaluation of foot lesions is required, and in diagnosing CODD in a flock the authors prefer to examine a number of affected sheep with a range of clinical presentations. As such the detailed description of lesions here and the grading system should aid in the diagnosis of CODD and in differentiating it from other lesions.
In this study, the distribution of lesions was not even—there being more grade 2 and grade 5 lesions represented and fewer grade 1 lesions. This may be due to the sampling strategy of preferentially selecting lame sheep for examination, or as is suspected, if the lesion grades form a continuum this may reflect that some stages of the disease progress more rapidly than others. Repeated observation of individuals with CODD over time may help to understand this.
For some time Bovine Digital Dermatitis (BDD) and CODD have been hypothesised to be the same disease but in different species (Demirkan and others 2001, Dhawi and others 2005, Duncan and others 2014). However, the typical clinical picture as evidenced here in sheep is strikingly different from that for cattle. As such, any detailed comparisons between lesion scoring systems for cattle, for example, Dopfer and others (1997), are difficult.
Given the small sample size, the radiographic changes presented here are examples only and may not be representative of all feet at each grade. In these examples, in early CODD lesions (grade 1) very little radiographic changes were evident. As the hoof horn was underrun, the damage to the foot became not only more extensive but progressed deeper into the tissues as well, leading to inflammatory bony changes on P3 and in some cases leading to extensive damage to P3.
These radiographs highlight the possible extent of the disease if it is unchecked, and may provide some explanation for why sheep can remain lame once healing has occurred. As treatment strategies are developed, these should focus on early identification of CODD and early intervention—so that the progression of the disease may be halted before it leads to extensive and potentially irreversible damage. It would also suggest that systemic rather than topical treatments may be more appropriate, particularly for grade 2–4 lesions due to the depth of the inflammatory changes and the possible penetration of infection to the deeper tissues.
Further work would examine the pathological and histopathological changes of the feet at these various grades to understand the mechanisms and pathophysiology of the disease better.
The changes in locomotion in affected sheep suggest pain is likely to be associated with CODD lesions, indeed there is an association between the locomotion score and the grade of disease. All sheep were locomotion scored during handling in pens in order to examine the sheep, and before foot examination to reduce bias. It is well known that on the basis of their status as a prey species, sheep can reduce the behaviours associated with pain when handled (Fitzpatrick and others 2006, Phythian and others 2013) and so in a field situation sheep may appear more lame than when gathered and handled. Unfortunately, due to practical constraints it was not possible to locomotion score individual sheep undisturbed in a field and then subsequently grade the lesion.
Grade 1 CODD lesions tended to show only mild lameness and sheep with these lesions may be difficult to observe when standing or walking, particularly in a group situation or when handling sheep in pens (median locomotion score 1).
In Angell and others (2014) 47.3 per cent of farmers reported that they did not know how CODD had arrived on their farm. However, a further 43.5 per cent reported that they thought CODD was introduced into their flocks following the purchase of infected sheep. It is therefore possible that sheep with a grade 1 lesion may not be noticed until infection has already spread to the rest of flock. This has important implications for flock biosecurity. Close inspection of the feet of all purchased animals, together with a period of isolation away from the rest of the flock would be recommended in order to identify any mild lesions that are not causing any locomotor changes. This would seem particularly important for naïve flocks due to the contagious nature of the disease (Davies and others 1999; Harwood and others 1997), the high prevalence seen on some farms (Angell and others 2014) and the current lack of effective treatment strategies.
Grade 1 lesions appeared to progress to grade 3 over time, and sheep with these lesions appear severely lame (median locomotion score 3). It is the authors’ view that this is likely to be due to the movement of the horn causing pinching of the underlying soft tissue, and the associated laminitis.
As would be expected, a greater degree of underrunning led to increased locomotion scores with CODD grade 3 lesions showing increased scores compared with grade 2 lesions. Shedding of the hoof horn led to a reduction in locomotion score which may indicate that this helped alleviate some of the pain. Interestingly all six farmers observed that sheep tended to recover faster if the underrun hoof horn was gently and carefully removed by trimming, taking care to avoid damage to the underlying soft tissue structures. This is consistent with other anecdotal observations of the disease (Harwood and others 1997).
During recovery the hoof horn regrew, although there was usually some deformation of the new horn growth and the affected digit was appreciably shortened. This suggests that the damage to the coronary band was not total thus allowing the horn to regrow. It is notable that some of the sheep with healed lesions remained lame, which may be due to damage to the deeper structures including the distal phalanx. Interestingly all the farmers reported that some individuals were lame for many weeks after regrowth and this may suggest irreversible damage to underlying structures or damage to nerve endings resulting in hyperaesthesia and allodynia (Lumb and Jones 1996), and is consistent with observations made by Scott (2010).
Contagious ovine digital dermatitis is a severe and debilitating disease of sheep that has a range of clinical signs. Lesions commence at the coronary band leading to underrunning of the hoof horn capsule dorsally and abaxially resulting in sloughing of the hoof horn capsule. Horn regrowth and recovery is possible although sheep may remain lame. The disease can cause severe damage to the soft tissues of the ovine foot and can lead to bony changes in the distal phalanx. Effective treatment and prevention strategies are urgently warranted in order to improve the welfare of sheep and the profitability of affected sheep farms.
The authors thank the farmers involved in the study for their compliance in providing their sheep for study. The authors also thank Leigh Sullivan, Soffi Jones, Lisa Wharton, Kyle Tindall-Reed, Brian Angell, Anna Angell, Victoria-Ann Moxon, Michael Sullivan, Daniel Bell and Erica Swan for their assistance with entering data on farms.
Provenance: not commissioned; externally peer reviewed
Funding This study was supported by a grant from the British Veterinary Association Animal Welfare Foundation. The funder had no role in study design; collection, analysis and interpretation of data; in writing the report; or in the decision to submit for publication.
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