Infectious Foot Rot in Small Ruminants
Phtlippa Gibbons
■ Epidemiology Lameness is a significant issue in small ruminant welfare and production. In the UK, lameness prevalence was estimated at 10.4%1 in 2004, with 80% of lameness caused by foot rot.2 In 2013 prevalence had decreased to 5.4%.3 In the United States, 20.4% of sheep producers reported lameness as an important issue, and 24% of producers treated ewes for lameness.4
■ Pathophysiology Two organisms are involved in ovine foot rot: anaerobic gram-negative bacteria Fusobacterium necrophorum, found in the environment and feces, and Dichelobacter nodosus, an obligate parasite of the foot.
It has been generally accepted that D. nodosus can survive in the environment (in feces, soil, or pasture) for only 10 to 14 days, which has influenced eradication protocols. However, survival up to 30 days has been reported,5,6 with prolonged survival in clay soils.5 Transmission occurs when mean daily temperatures exceed 10° C (50° F) and rainfall is greater than 50 mm per month.7 However, in the UK foot rot has been reported year round when environmental temperatures are outside these parameters.8 Transmission can also occur during periods of housing in warm, wet bedding.7 Transmission of foot rot from ewes to lambs has been shown to be primarily through D. nodosus in the environment rather than direct transmission.9Historically, F. necrophorum was thought to be the causative agent of interdigital dermatitis (or scald), with secondary infection with D. nodosus causing the sloughing of the hoof wall seen in foot rot cases.7 Pasture conditions resulting in excoriation of the interdigital skin and maceration due to wet conditions predispose animals to developing interdigital dermatitis.7 In recent studies, D.
nodosus has been shown to have a primary role, with F necrophorum secondary.10,11 Current literature suggests that interdigital dermatitis and foot rot should be treated as one disease. Ten serogroups of D. nodosus have been identified, some of which are virulent strains. Virulence factors of D. nodosus have been identified as type IV fimbriae and AprV2 proteases.12Foot rot caused by F. necrophorum and D. nodosus has also been reported in cattle, horses, pigs, deer, and mouflon.13 There is little published information about the disease in goats,14 but foot rot is a reported cause of lameness in goats.15 Overgrown hoof wall is more common in goats than sheep.15 Treatment with oxytetracycline is reportedly effective in goats.16
■ Clinical Signs and Differential Diagnoses Diagnosis of foot rot is by examination of the feet. This is commonly performed by producers. Studies investigating interobserver agreement for lameness diagnosis in sheep achieved good levels of reliability when both experienced and inexperienced observers were assessed.17 Ovine foot rot infection is characterized by lameness, foul-smelling interdigital dermatitis, and sloughing of the hoof wall as a result of separation of the hoof horn from sensitive laminae.11 Disease can be characterized as benign, intermediate, or virulent.7 Australian studies typically define foot rot as benign or virulent, according to determination of the virulence factors of D. nodosus. British studies typically characterize the disease according to clinical signs and lameness severity. Virulent D. nodosus has been detected in the feet of nonlame sheep, however.1 Interdigital dermatitis (scald) is a milder form of disease primarily limited to the interdigital skin and without a foul odor.7 Foot rot should be distinguished from contagious ovine digital dermatitis (CODD), which has low reported prevalence in the United States and results in severe lameness and underrunning of the hoof wall at the coronary band, ultimately resulting in avulsion of the hoof capsule.
Treponeme bacteria are the presumed causative agent for CODD. Due to treatment differences for the two conditions, identification of the cause of lameness is important.18 Confirmation of foot rot is achieved by laboratory testing; however, culture of D. nodosus can be challenging due to the fastidious nature of the bacteria. Gelatin gel, elastase, and intA PCR were used in one study,19 but agreement between the three tests was low. Real-time PCR has also been used in individual20 and pooled samples.21 Quantitative PCR showed poor diagnostic specificity compared to the elastase test for one study.22■ Treatment and Prognosis Historically, foot trimming and topical administration of antibiotics formed the major treatment and control measures for foot rot; however, foot trimming is no longer recommended as a treatment for foot rot due to prolonged recovery in trimmed sheep.23,24 The number of ewes bleeding post foot trimming has been associated with higher prevalence of lameness.3 Oxytetracycline administered parenterally is the most commonly reported antimicrobial treatment.7,23-25 Oxytetracycline is not labeled for treatment of foot rot in sheep in the United States; therefore regulations for the extralabel use of antimicrobials and withdrawal times should be followed. Sheep treated with gamithromycin showed a significant reduction in foot rot-affected feet and severity of lesions compared to those treated with oxytetracycline in a nonblinded study in Germany.25 Whole flock treatment with Micotil (tilmicosin) was investigated in the UK. Treatment reduced but did not eliminate disease from farms. The authors did not recommend whole flock treatment with Micotil due to the failure to eliminate disease, along with concerns about use of a critically important antimicrobial.26 Gamithromycin used on a whole flock level was successful but cannot be recommended for the same reasons.27 Florfenicol was used on a single flock of ewes in Germany in a targeted, selective fashion, and resolution of lesions was achieved in 96% of animals.28 Penicillin and dihydrostreptomycin combination has also been used in countries where it is available.23
Topical antibiotics (oxytetracycline) have been used to treat interdigital dermatitis successfully if dry conditions are maintained after treatment.23 In a single flock study in the UK, prompt administration of parenteral oxytetracycline and topical tetracycline reduced lameness scores and improved production.
Ewes had higher body condition scores and raised more lambs compared to those treated with trimming and topical antimicrobials.29■ Prevention and Control Elimination of foot rot has been successfully achieved in Australia,30 Norway,31 and Switzerland.32 The Australian eradication protocol used a combination of total destocking, inspection and culling of clinically infected animals, treatment with antibiotics, and culling and foot bathing.30 Foot bathing took the longest time to achieve elimination and was the most labor intensive approach.30 The Swiss eradication model involved careful claw trimming, weekly foot bathing in 10% zinc sulfate, and isolation or culling of nonresponders.32 No antimicrobials were used. A similar protocol was used in Norway.31 In the UK, a six-step method has been promoted; it involves treating sheep within 3 days of becoming lame; foot inspection without foot trimming; correct diagnosis; treatment of affected sheep with parenteral and topical antibiotics, not trimming; identification of treated sheep; and culling of chronic cases.33 Eradication of the disease has been more easily achieved where there are periods of nontransmission (dry, hot weather); therefore eradication in
23
wet, temperate climates is challenging.23
Foot bathing has been used for both treatment and control. Formalin at 2% to 3%, copper sulfate at 5%, antimicrobials, and zinc sulfate at 10% have been used.23 To be effective, foot baths should be cleaned regularly and sheep should stand on a hard surface following bathing. Concerns about foot bathing include the use of formalin in meat-producing animals, the sensitivity of sheep to copper,34 and the use of antimicrobials in an extralabel fashion.23 Higher concentrations of formalin can cause cracking of the hoof wall due to overhardening.23 Due to these concerns, zinc sulfate has been the most widely promoted.
Foot bathing, however, is time consuming (2 to 20 minutes of contact time for zinc sulfate, depending on concentration) and should be repeated at least once a week for 3 weeks to be effective. Foot bathing has been shown to be economically feasible if minimized to treatment and prevention of interdigital dermatitis rather than treatment of foot rot.35Vaccination has been used in both treatment and control of ovine foot rot. Commercially prepared vaccinations are not available in the United States. Vaccines available in other countries include recombinant fimbrial vaccine to 10 strains of D. nodosus. Monovalent and bivalent fimbrial vaccines are also available. Vaccination programs are most effective when used during a period of high-risk transmission.23 Commercially available vaccines have been shown to protect for only 10 weeks, whereas monovalent and bivalent vaccines have been shown to be protective for longer periods. This effect is presumed to be due to antigenic competition.36 Where multiple serogroups are present in a flock, antigenic competition can be overcome by sequentially targeting the serogroups with different bivalent vaccines every 3 months.36 A contraindication of vaccination and simultaneous treatment with the anthelmintic moxidectin has been reported.37
Studies have shown that susceptibility to foot rot has some 3839
heritability38,39; however, there is also evidence to suggest that the infection rate and environment (bacteria die more rapidly in hot, dry conditions) are more significant than heritability in control of the disease.40
Selenium supplementation has been suggested to increase speed of resolution of foot rot lesions, although in a preventative model this finding was not replicated when selenium was fed at supranutritional levels.41,42