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Advances in the Control of Foot Rot in Sheep
Advances in Sheep and Goat Medicine
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Advances in the Control of Foot Rot in Sheep Cleon V. Kimberling, BS, DVM, MPH, * and Robert P. Ellis, PhDt
Foot rot is a contagious disease of sheep and goats that is transmitted by Bacteroides nodosus. Foot rot may occur in cattle, deer, and possibly other ruminants, although the clinical severity in these animals is much less than in sheep. The disease is characterized by a chronic bacterial infection that is confined to the epidermal tissues of the interdigital skin and horn of the hoof. Contagious ovine foot rot is one of the most limiting diseases of sheep production world-wide. Many producers in the United States have quit sheep production owing to their inability to control foot rot. Australia, the country with the greatest number of sheep in the world, regards foot rot as their most economically important contagious disease of sheep.17 Although tremendous expenditure of research, money, and time has provided new and rewarding control capabilities, the disease remains elusive and extremely difficult to eradicate. DEFINITION AND ECONOMIC IMPACT Ovine contagious foot rot is a complex disease caused by the interaction of two bacteria- Bacteroides nodosus and Fusobacterium necrophorum - and is complicated by macro- and microenvironments, genetics, and micronutrient imbalances that compromise the integumentary and immune systems. Unlike many other diseases, which are caused by individual infectious agents, the collaboration of B. nodosus and F. necrophorum is required to produce clinical disease. F. necrophorum is ubiquitous in the animals' environment and the necessary precursor to the establishment of the invasive B. nodosus. B. nodosus is the essential organism for producing foot rot. Because B. nodosus is a strict anaerobe and is solely dependent on the oxygen-free lesions of the sheep's foot for survival, eradication is possible. From the Colorado State University College of Veterinary Medicine and Biomedical Sciences, Fort Collins, Colorado *Extension Veterinarian, Veterinary Diagnostic Laboratory tProfessor, Veterinary Diagnostic Laboratory and Department of Microbiology Veterinary Clinics o/North America: Food Animal Practice-Vol. 6, No.3, November 1990
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Temperature and moisture play an important role in transmission and invasion of the organism. Therefore, most outbreaks occur during the season of high rainfall, warm temperature, and lush pasture growth. The disease occurs in the temperate climate of all sheep-producing countries in the world. Foot rot was endemic in Britain during the 18th century and was identified in most other major sheep-producing countries during the 19th century.17 The exact economic impact of the disease is impossible to calculate. A monetary figure can be assigned to the additional labor, drug and treatment costs, additional feed, and other expenses, but it is impossible to accurately measure the losses from decreased meat and wool production and increased expenses of other necessary management practices. In a foot rot outbreak involving 1800 Colorado range ewes, 42% were treated at least once. The additional labor, feed, and medication costs were $27.78 for each ewe in the flock. The death loss and loss of production was estimated at an additional $60.00 per head. 19 In an Idaho study, the treatment cost of foot rot in a range flock of 13,000 ewes was calculated to be $4.41 per ewe from 1980 to 1982. Treatment costs represented only 3% of the total expenses of the disease. 3 In an Australian trial, wool-production losses alone in Merino sheep affected with foot rot, compared with unaffected sheep, were estimated at $42.50 per head. 17 In a decision-tree analysis of various treatments and management combinations,41 it was determined that treatment, although costly, is better than no treatment, even when prevalence is very low. The increased profit per ewe in an infected herd was predicted to be $1.79 (at a 10% foot rot prevalence) to $6.45 (30% prevalence) more when sheep were treated with 10% zinc sulfate than when sheep were not treated. Thus, although treatment is expensive, it is theoretically more economic than "living with" the disease. ETIOLOGY AND PATHOGENESIS Etiology B. nodosus and F. necrophomm, pathogenic synergists, cause contagious foot rot. 29 Other organisms often enter the lesions and play an unknown role in the pathogenesis. Although F. necrophomm plays a major role in the pathogenesis,21 the severity of the lesion depends upon the virulence of B. nodosus. B. nodosus is a nonsporing, nonmotile, noncapsulating, granular, gram-negative, anaerobic bacillus with bulbous ends. The pili on the cell membrane are associated with virulence and antigenicity. 22,27,32,50,51 There are more than 22 B. nodosus serogroups, each exhibiting varying degrees of virulence. 49 Pathogenesis Beveridge 2 pioneered the work on the etiologic agents, pathogenesis, and epidemiology of contagious foot rot. During his investigations, he observed that the organisms currently classified as B. nodosus and F. necrophorum were synergistic in producing virulent foot rot. He also observed that foot rot of greater severity was more consistently produced when Spirochaeta penortha was present. More recent studies by Hine 28 have shown that apart from B. nodosus and F. necrophomm, a filamentous rod-shaped bacterium is also associated with F. necrophomm in the tissues and appears to have the ability to penetrate keratinized tissues directly. The growth characteristics are apparently consistent with those of the motile organism described by Beveridge. The findings of these workers indicate that foot rot is a complex disease caused by the synergistic actions of F. necrophomm and other organisms limited by the essential transmitting and virulence agent B. nodosus. Edgerton et
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al lS concluded that following colonization of macerated interdigital skin, F. necrophorum facilitates infection with B. nodosus, probably by inducing hyperkeratosis and parakeratosis. This results in crevices where anaerobic bacteria can survive and multiply. F. necrophorum, because of its invasiveness and elaboration of exotoxin, is responsible for most of the inflammation and initiation of tissue damage. B. nodosus has minimal inflammatory capabilities but initiates the invasion and extension of the lesion into the hoof matrix. B. nodosus is able to persist in lesions for long periods, thereby sustaining the infection. It also produces a heat-stable soluble factor that enhances the infectivity and invasiveness of F. necrophorum, a normal inhabitant of the sheep intestinal flora that is ubiquitous in the environment. The pathogenesis of contagious foot rot begins with transmission of B. nodosus from the environment to macerated or scald-affected interdigital skin. At the skin-horn junction near the axial bulbar notches, F. necrophorum and possibly other unidentified organisms begin the disease process by colonizing the moist epidermal surface; only then does B. nodosus, as the second step, adhere to the host tissue, colonize the sites on the feet that have lowered oxygen tension, penetrate the tissue and, owing to the pili, colonize the epidermis of the hoof. By action of its powerful keratinolytic protease, B. nodosus liquefies the cells of the stratum granulosum and stratum spinosum and thus cleaves the cells and separates the horn corium from the basal epithelium and derma. 29 The ensuing waves of F. necrophorum account for the strong and damaging inflammation. The degeneration, detachment, and liquefactive digestion of partially keratinized cells of the stratum lucidum and stratum spinosum, as well as formation of fissures, sinuses, and necrotic foci in the keratinized horn, appear to be directly related to the presence of B. nodosus. The ability of B. nodosus to maintain itself for long periods in apparently healed lesions and the recurrent waves of F. necrophorum associated with suitable microenvironmental changes probably account for the recurrent episodes of severe clinical foot rot. Host Susceptibility Parker et aP7 in the United States and Skerman45 in Australia have shown that resistance to foot rot is a genetically heritable trait in selected Targhee and Romney sires. Australian workers 14,17,45 reported variability between breeds, with the British-breed sheep being more resistant than the Merino. Age also appears to be a factor. As age increases, resistance apparently decreases. There is a wide spectrum of resistance within any sheep population; some individuals withstand repeated challenges, whereas others succumb to acute infection and may heal spontaneously or become clinically infected carriers. Transmission Infective material is transferred directly from an exposed lesion onto soil, thereby providing a contaminated environment for the feet of other sheep. Exposure of susceptible sheep is provided by the nature of sheep to congregate in groups during the heat of the day, trail single file along paths to and from water, or use a common watering or feeding area. B. nodosv~, because it is anaerobic and oxygen sensitive, dies rapidly once it is away from the lesion of its host. The organism lives no longer than 4 to 5 days in contaminated material. 31 It is totally host-dependent for multiplication and long-term survival. Mechanical transmission to other farms or ranches on various fomites such as boots, vehicle tires, feet of animals other than sheep, and so on is possible but improbable. Owing to the highly contagious nature of the organism, infected sheep are the most probable mode of spread from farm to farm. Mechanical
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transmission via instruments used in paring hooves is possible; therefore, they should be disinfected between sheep. I Any management practices that tend to concentrate sheep into small areas such as high stocking rates on irrigated pastures, access to streams or watering facilities, feedlots, common trails, and so on increase the risk and likelihood of transmission. Predisposing Environmental Factors Conditions of high moisture, warm temperatures, lush pasture growth, and a susceptible host, together with a source of infection, favor outbreaks of the disease. In temperate climates, the spread and outbreaks of foot rot are usually associated with the rainy season and a mean ambient temperature above 10°C, or 50°F. There are areas of the northwestern and southeastern United States that remain ideal for foot rot spread throughout the year, whereas foot rot is a seasonal disease, maintained in the feet of chronically infected animals, in the midwest and northeast. The western mountain and intermountain range areas, although extremely arid, experience severe localized outbreaks owing to environmental niches within these vast expanses that are moist and have lust plant growth, which tends to attract concentrations of animals to those habitats. Some range operators may use common trails and working facilities and overlap on grazing permits. Stray animals may enter other Hocks because, owing to lameness, the strays were unable to keep up with the parent Hock. The extremely contagious characteristics of B. nodosus play an important role in the transmission of foot rot from sheep to sheep within the Hock or between Hocks. Unfortunately, most foot rot is introduced through the purchase of infected animals. Under ideal transmission conditions, 70% or more of an unvaccinated Hock will develop foot rot in an outbreak if no prophylactic precautions are taken. 15 Soil moisture appears to be the limiting factor in transmission. Beveridge l noted that foot rot was much more prevalent on improved fertilized pasture with lush growth containing clover than on natural pasture of lighter carrying capacity. The improved and irrigated pastures create an ideal microenvironment for the spread of foot rot - first, by concentrating animals and, second, by allowing better retention of surface moisture. Transmission of foot rot ceases as the total environment dries out, with the consequent dehydration of the interdigital skin, although there may be sufficient moisture for continued plant growth. 25 As noted previously, small niches of moist to muddy soils, such as that found at waterholes, stream crossings, and water troughs, also serve as very successful areas for transmission. Reservoir of Infection After foot rot occurs, there is chronic disease, inapparent infection, or complete recovery. An individual sheep that completely recovers does not serve as a source of infection for other susceptible sheep. In any outbreak, natural healing is a normal feature, with a variable proportion of the infected sheep remaining chronically or inapparently infected. Chronically infected animals do not pose a particular threat, because they can be easily identified and eliminated, whereas the inapparent or symptomless carrier constitutes a risk to the remainder of the population. In one type of inapparent state, the infection may be in small foci under healthy horn, which can only be identified by careful paring. Some of these cases can be identified by a slightly misshapen hoof. If undetected, these pose a potential threat of reinfection if the sequestered infection breaks out to the surface. Benign strains may be more subtle in their clinical manifestation and, therefore, more difficult to detect and eliminate, with the inapparent carrier being the reservoir for reinfection when conditions become ideal.
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In Australia, several benign strains of B. nodosus have been isolated from farmed red deer and cattle. In passage to sheep, these strains have caused benign foot rot. 30,46,48,55,56 Natural transmission of virulent B. nodosus from sheep to cattle has not been successful. 30 Australian workers consider it highly probable that cattle are a reservoir for benign foot rot of sheep,40 but in relation to virulent foot rot it is unlikely that cattle constitute a major risk to sheep.40 Because goats can be infected with virulent and benign strains, they can be a potential reservoir. 5,52 In the United States, deer, elk, bighorn sheep, and goats have not been investigated, and their role as reservoirs is unknown. In endemic areas, sheep remain the most likely carriers. Clinical Signs The clinical signs observed in sheep affected with foot rot depend on a variety of factors, including the virulence of the organism, the climatic environment, the health or trauma to the interdigital skin, and a number of host factors. Although three types of foot rot are described in Australian literature 19,54 (virulent, intermediate, and benign), there are basically two clinically recognizable forms of foot rot in sheep: virulent and benign. InHammation of the interdigital skin is seen with both forms. Virulent foot rot is characterized by extensive separation, which commences at the heel, extends to the sole and toe, and frequently involves separation of the abaxial wall, with the formation of a distinctive, foul-smelling, necrotic exudate. Benign foot rot (a form of scald) is characterized by occasional separation of the horn of the heel bulbs and posterior sole region, but there is a limited accumulation of necrotic material under the separated horn. 12,54 Benign foot rot is further characterized by causing only a mild lameness that rapidly regresses following topical treatment or after the onset of dry environmental conditions. 12 In comparison, virulent foot rot causes severe lameness that persists and requires intensive treatment to alleviate the symptoms. In any severe outbreak of virulent foot rot, a wide spectrum of clinical involvement may be seen. In a Colorado study, Ellis et al 19 developed a scoring system of 0 - 3 for assessing severity, which correlates closely with the virulent, intermediate, and benign system. A score of 0 indicates no foot rot, 1 indicates an initial lesion of the interdigital skin between the toes or at the heel, 2 indicates the lesion has advanced with some underrunning of the sole, and 3 indicates there is underrunning of the sole and abaxial wall with a foul-smelling exudate. It is possible to see all four conditions on one individual. CONTROL AND ERADICATION Contagious foot rot in sheep causes reduced weight gain and wool yield (and death), which results in economic losses to sheep producers world-wide. Many treatment regimens and preventive measures for this disease have been proposed. Before deciding which method of prevention or treatment is most appropriate for a given Hock situation, sheep owners and veterinarians should consider the cost and the likely economic benefit of the various treatments and control procedures. 41 Because foot rot is a relatively superficial bacterial infection localized in the zone between the keratinized horn and the avascular living epidermal tissues of the hoof and still accessible to substances diffusing from the blood stream, several therapeutic options are available. Surgical paring of the hoof to expose the lesions followed with topically applied antibacterial agents, although labor intensive and time-consuming, is an effective means of treatment. To be effective, the surgical preparation of the
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foot is very important. Each foot must be thoroughly examined and meticulously pared. The full extent of the infection must be exposed by removing all underrun sole and wall covering the lesion. 35 Proper and adequate restraint are essential to an effective paring procedure. A simple manual tip-over restraining device can be built, or more sophisticated, commercially available restraining devices can be used. Whatever the device, it is essential that all feet are easily accessible. To ensure adequate and proper paring, a good set of hand shears with good blades and a sharp paring knife are essential. Hemorrhage is undesirable because it may mask the operative field and interfere with the action of the topical agent. It is better not to be too conservative, because insufficient paring may leave pockets of infection. 39 Paring should be done from heel to toe to minimize bleeding. 39 Following paring, topical bactericidal agents are applied to the exposed diseased tissue. Quaternary ammonium antiseptic solutions, iodophor antiseptic solutions, iodine, or 10% zinc sulfate in water give excellent results. 6 Cross6 showed that a 10% zinc sulfate solution was more effective than a 10% formalin or a 10% copper sulfate solution. For best results, the sheep should be kept on a dry surface (concrete or board) for at least 1 hour following topical treatment. 2,38,47 Footbathing When large numbers of sheep are involved, footbathing is a practical alternative to individual treatment. Over the years, copper sulfate and formalin have been the standard materials used in footbaths. More recently, a 10% to 20% zinc sulfate solution with 2% sodium lauryl sulfate has proved as effective as formalin or copper sulfate. Footbaths containing zinc sulfate have been shown to be effective, safe, practical, and economic. Cross and Parker8 demonstrated that daily footbathing in 10% zinc sulfate for 30 days, without paring, greatly reduced the number of clinical cases. Malecki and McCausland33,34 showed that, in vitro, the anionic surfactant sodium lauryl sulfate increased the penetration of zinc sulfate into the hoof approximately sixfold, whereas formaldehyde did not penetrate at all. Bulgin et al 4 found that footbathing in 10% zinc sulfate (containing 0.2% heavy-duty laundry detergent with nonionic surfactants) for 1 hour at IO-day intervals was an effective treatment of chronic cases without the necessity of foot paring. A 10% zinc sulfate - surfactant solution with a 10 to 30 minute soak at 5-day intervals appears to be ideal for curing interdigital and benign cases of foot rot. The zinc sulfate solution can be prepared using fertilizer-grade zinc sulfate. The rough formulation of a 10% ZnS04 solution is BIb ZnS04/10 gal of water. Fertilizer grade ZnS04 is usually 35.5% or 22.7% zinc. Therefore, to obtain a 10% solution, 22.5 pounds of 35.5% ZnS04 or 35 pounds of 22.7% ZnS04 should be used per 10 gallons of water . Warm water greatly enhances the solubility of the ZnS04' A satisfactory wetting agent such as sodium lauryl sulfate should be added at a 0.2% vol:vol concentration (approximately two thirds of a cup per 20 gallons of water). Although this treatment has a high curative rate on severe and chronic cases, the effectiveness is improved with paring. 4,35,36 In some cases, improper paring can be detrimental to the cure rate. Of the three products currently being used (zinc sulfate, copper sulfate, and formalin) for footbath solutions, zinc sulfate has no irritating fumes, is less toxic, does not stain the wool, and is nonirritating to the skin. Parenteral Antibiotic Therapy Numerous trials have been conducted on parenteral antibiotic treatment of contagious foot rot. In a study ~onducted by Gradin and Schmitz,24 it was found
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that penicillin was the most effective of a wide range of antimicrobials tested, including the newer antibiotics cephalosporin and clindamycin. Harris 26 observed that when using parenteral antibiotics the cure rate was improved and subsequent assessment was easier and more accurate if the sheeps' feet were thoroughly pared. In wet conditions, better results were obtained if sheep were housed on slotted Hoors in a dry environment for 24 hours after treatment. 11 An interdigital subcutaneous injection of penicillin-streptomycin was no more effective than the intramuscular route. 6 From all of the trials and field observations conducted, it appears that parenteral antibiotics have a fairly high cure rate and have the added advantage of reaching the undetected sequestered lesion. The disadvantage of mass parenteral antibiotic therapy is the tremendous expense without complete cure or eradication. This method of therapy is probably suited for select individuals for which careful hoof paring and close observation is possible. There is also the potential human health hazard of drug-resistant organisms and food safety. The report by Demertzis and Mills, 9 that healing of cases of bovine infectious pododermatitis in bull calves could be attributed to a daily intake of zinc as a drench, stimulated investigations into oral zinc therapy for prevention and cure of ovine contagious foot rot. A wide spectrum of dosage ranges was fed over periods extending to 6 months. It was concluded from these studies that oral zinc was of no practical benefit in reducing the prevalence or severity of B. nodostlS infections in treated animals and did not enhance the resistance of sheep to foot rot. 6 ,7,9,10,16,24,44 Immunization Immunization can provide the most efficient and cost-effective control of foot rot provided an effective vaccine is used. Following the release of Footvax (Coopers Animal Health Australia, formerly ICI Australia Pty) in 1981 and Pro-vac (Coopers Animal Health Australia, formerly Wellcome Australia Pty) in 1982, United States researchers in Idaho, California, and Colorado conducted efficacy trials. 3 ,19,23 To license a commercial vaccine in Australia, the cure rate must be at least 65% with a protection rate of 70% at 6 and 12 weeks, respectively, after vaccination. With cure rates, there must be at least 20% affected initially, and for protection rates, 30% of infected sheep in the unvaccinated control group must be infected at the time protection is measured. Although the vaccine provides prophylactic and preventive benefits, it does not provide complete protection and must be used with other management practices of trimming, foot soaking, and vigorous culling if foot rot is to be eliminated from a flock. Besides being expensive, the vaccine produces granulomas and abscesses at the injection site (30%-70%), which usually resolve in a few weeks and are of only cosmetic importance. In the continuation of the Colorado study, where vaccination was carried out annually at 4 to 6 weeks prior to the period of highest transmission, the incidence was reduced from an initial infection rate of 15% in April 1985 to 0.2% in July 1986. The reduction was greatly enhanced by paring, footbathing, and culling. Failure to cull a few chronically infected ewes resulted in an outbreak in 1987 involving 15% of the flock. Recently (June 1989), with increased paring and culling, the incidence in this flock is back down to 2.4% (Ellis and Kimberling, unpublished results). These observations further indicate that vaccination is only one element of a control program. Ideally, it should be possible to effectively control foot rot using vaccines, without the need of the labor-intensive operations of foot paring and footbathing. Research is currently being conducted in the United States and Australia on recombinant DNA vaccines. The initial trials are extremely promising, with increased efficacy and reduced production costs. 18,53
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Control and Eradication With our current knowledge, it is safe to say that foot rot can be eradicated from a population of sheep. A successful program is dependent on a number of factors, the most critical being the commitment and understanding of contagious foot rot by management and all persons involved with the operation. This involves a thorough understanding of the disease and the highly contagious properties of B. nodosus. All diseases, including contagious foot rot, have similar steps in the infectious process. Understanding the individual characteristics of the organism, how it survives in the host, how it escapes from the host, its survivability in the environment, the properties of transmission, and the susceptibility factors of the new host are all integral in control of foot rot. In contagious foot rot of sheep, we know that B. nodosus is the limiting organism for infection. It has the capability of surviving in walled-off lesions in the misshapen hoof for extended periods of time and the ability to change from a latent, inapparent infection to an acute, virulent infection when the microenvironment is favorable. Outside the host, survival is short (4 to 7 days) and dependent on a mean ambient temperature of 50°F (10°C) with adequate humidity and moisture. The organism is susceptible to penicillin via parenteral injections or can be killed by direct contact with zinc sulfate, copper sulfate, or formalin. The more than 22 serotypes of B. nodosus have different invasive, virulence, and immunogenic properties. The primary reservoir is sheep, with goats, cattle, and deer being infected but playing a minor role or no role whatsoever in the spread of the disease. There are genetic differences between breeds and within breeds, with the Merino being highly susceptible and the Romney exhibiting some degree of resistance. Selected sires have been identified that produce resistant offspring. The resistance of the host can definitely be increased with available vaccines. None of the available vaccines will give absolute protection, but with paring, footbathing, and culling, they will enhance a control and eradication program. New methods of vaccine development and delivery are encouraging and should enhance our ability to control and eradicate foot rot. Taking the known facts about the organism plus the interaction of the environment and the host, we can outline a suitable plan to prevent, control, or eradicate the disease. The plan must be individually tailored for each enterprise, because no two operations have identical environments, facilities, or management. An assessment of prevalence and the economic impact on production will determine if control or eradication is the most cost-effective program. The basic steps are the same regardless of the plan. SUMMARY All cases of foot rot, whether acute, chronic, benign, or inapparent, must be identified. If the outbreak is severe and production losses warrant, each foot of each animal must be examined thoroughly. Proper handling facilities and equipment, adequate light, and dry working conditions are needed to properly examine each foot. Infected sheep must be separated from the clean Hock. Following extensive treatment, these animals must be diagnosed as free from the disease before returning to the clean Hock. Animals that do not respond must be culled from the Hock. Although copper sulfate and formalin are effective materials for footbathing, zinc sulfate is equally effective and does not irritate the skin, eyes, or lungs as does formalin, or stain the wool as does copper sulfate. A 10% zinc sulfate
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solution with a nonionic surfactant is an effective footbathing or foot soaking solution. The cure rate is improved by a thorough foot paring and a foot soak of at least 30 minutes. A number of treatment options along with formulations are outlined in the 1988 edition of the Sheep Production Handbook of the Sheep Industries Development Program, Inc, 6911 Yosemite, Englewood, CO 80112.
REFERENCES
1. Beveridge WIB: Foot-rot in sheep: A transmissible disease due to infection with Fusifonnis nodosus. Studies on its cause, epidemiology, and control. J Counc Sci Ind Res, Bull 140:14, 1941 2. Beveridge WIB: Bacterial diseases of cattle, sheep, and goats. Canberra, Aust Govt Pub Ser, 108:178, 1983 3. Bulgin M, Lincoln SD, Lane VM, et al: Evaluating an ovine foot-rot vaccine. Vet Med 80:105, 1985 4. Bulgin MS, Lincoln SD, Lane VM, et al: Comparison of treatment methods for the control of contagious ovine foot rot. J Am Vet Med Assoc 189:194, 1986 5. Claxton PD, O'Grady KC: Foot rot in goats and characterization of caprine isolates of Bacterioides nodosus. In Stewart DJ, Peterson JE, McKern NM, et al (eds): Foot rot in Ruminants. Proc Workshop, Melbourne, 1985. Glebe, NSW, csmo Div Anim Health/Aust Wool Corp, 1986, p 119 6. Cross RF: Response of sheep to various topical, oral, and parenteral treatments for foot rot. J Am Vet Med Assoc 173:1569, 1978 7. Cross RF, Parker CF: Oral administration of zinc sulfate for control of ovine foot rot. J Am Vet Med Assoc 178:704, 1981 8. Cross RF, Parker CF: Zinc sulfate footbath for control of ovine foot rot. J Am Vet Med Assoc 178:706, 1981 9. Demertzis PN, Mills CF: Oral zinc therapy in the control of infectious pododermatitis in young bulls. Vet Rec 93:219, 1973 10. Demertzis PN, Spais AG, Papasteriadis AA: Zinc therapy in the control of foot rot in sheep. Vet Med Rev 1:101, 1978 11. Egerton JR, Parsons on 1M, Graham NPH: Parenteral chemotherapy of ovine foot rot. Aust Vet J 44:284, 1968 12. Egerton JR, Parsonson 1M: Benign foot rot-a specific interdigital dermatitis of sheep associated with infection by less proteolytic strains of Fusifonnis nodosus. Aust Vet J 45:345, 1969 13. Egerton JR, Roberts DS, Parsonson 1M: The aetiology and pathogenesis of ovine foot rot. I. A histologic study of the bacterial invasion. J Comp Pathol 79:207, 1969 14. Egerton JR, Morgan m: Foot rot in vaccinated and unvaccinated sheep. I. Incidence, severity, and duration of infection. Vet Rec 91:447, 1972 15. Egerton JR, et al: Onset and remission of ovine foot rot. Aust Vet J 60:334, 1983 16. Egerton JR. Laing EA, Mulley RC: Failure of oral zinc therapy to alleviate Bacteroides nodosus infection in cattle and sheep. Aust Vet J 62:85, 1985 17. Egerton JR, Yong WK, RiHkin GG: Foot Rot and Foot Abscess of Ruminants. Boca Raton, Florida, CRC Press, 1989, p 7 18. Egerton JR, et al: Protection of sheep against foot rot with a recombinant DNA-based fimbrial vaccine. Vet MicrobioI14:393, 1987 19. Ellis RP, et al: The efficacy of Footvax in the control of foot rot. Sheep Industry Development Res Dig, Winter 1986, p 7 20. Emery DL, Stewart DJ, Clark BL: The structural integrity of pili from Bacteroides nodosus is required to elicit protective immunity against foot rot in sheep. Aust Vet J 61:237, 1984 21. Emery DL, et al: Cultural characteristics and virulence of strains of Fusobacterium necrophorum isolated from the feet of cattle and sheep. Aust Vet J 62:43, 1985 22. Every D, Skerman TM: Surface structures of Bacteroides nodosus in relation to virulence and immunoprotection of sheep. J Gen Microb 129:225, 1983
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23. Glenn J, Carpenter TE, Hird DW: A field trial to assess the therapeutic and prophylactic effect of a foot rot vaccine in sheep. J Am Vet Med Assoc 187:1009, 1985 24. Gradin JL, Schmitz JA: Susceptibility of Bacteroides nodosus to various antimicrobial agents. J Am Vet Med Assoc 183:434, 1983 25. Graham NPH, Egerton JR: Pathogenesis of ovine foot rot: The role of some environmental factors. Aust Vet J 44:235, 1968 26. Harris DJ: Field observations on parenteral antibiotic treatment of ovine foot rot. Aust Vet J 44:284, 1968 27. Hindmarsh F, Fraser J: Serogroups of Bacteroides nodosus isolated from ovine foot rot in Britain. Vet Rec 116:187, 1985 28. Hine PM: Ovine Foot rot: Histopathology of a synergistic disease. In Hill MJ (ed): Models of Anaerobic Infection. The Hague, Martinus Nijhoff, 1984, p 85 29. Kimberling CV: Jensen and Swift's Diseases of Sheep. Philadelphia, Lea & Febiger, 1988, p 317 30. Laing EA, Egerton JR: The occurrence, prevalence, and transmission of Bacteroides nodosus infection in cattle. Res Vet Sci 24:300, 1978 31. Laing EA, Egerton JR: Some aspects of B. nodosus infection in cattle. In Ovine Foot rot, Rep Workshop, University of Sydney, May 3, 1981, p 195 32. Lee SW, Alexander B, McGowan B: Purification, characterization, and serologic characteristics of Bacteroides nodosus pili and use of a purified pili vaccine in sheep. Am J Vet Res 44:1676, 1983 33. Malecki JC, McCausland IP: Improvement of topical chemotherapy of ovine foot rot by increasing the penetration of therapeutic agents. In Ovine Foot rot, Rep Workshop, University of Sydney, 1981, p 165 34. Malecki JC, McCausland IP: In vitro penetration and absorption of chemicals into the ovine hoof. Res Vet Sci 33:192, 1982 35. Malecki JC, McCausland IP, Lambell R: A new topical treatment for foot rot. Proceedings No. 67, Sheep Production and Preventive Medicine, University of Sydney, 1983, p 63 36. Malecki JC, Coffey L: Effectiveness of treatment programs based on footbathing with a zinc sulphate formulation for virulent Bacteroides nodosus infection in sheep. In Stewart DJ, Peterson ]E, McKern NM, et al (eds): Foot Rot in Ruminants. Proc Workshop, Melbourne, 1985. Glebe, NSW, csmo Div Anim Health-Aust Wool Corp, 1986 37. Parker CF, Cross RF, Hamilton KL: Genetic resistance to foot rot in sheep. Annu Proc Sheep Vet Soc 9:16, 1985 38. Penny RHC: The topical application of 10% chloramphenicol in spirit in the treatment of foot rot in sheep. Br Vet J 11:125, 1985 39. Pryor WJ: The treatment of contagious foot rot in sheep. Aust Vet J 30:385, 1954 40. Richards RB, Depiazzi LJ, Edwards JR, et al: Isolation and characterization of Bacteriodes nodosus from foot lesions of cattle in western Australia. Aust Vet J 56:517, 1980 41. Salman MD, Dargatz DA, Kimberling CV, et al: An economic evaluation of various treatments for contagious foot rot in sheep, using decision analysis. J Am Vet Med Assoc 193:195, 1988 42. Sheep Industry Development Handbook, Health Chapter. Englewood, CO, American Sheep Industry Association, 1988 43. Sinclair AN: Studies on contagious foot rot of sheep. Aust Vet J 33:202, 1957 44. Skerman TM, Millar KR, Sheppard AD, et al: Failure of orally administered zinc to prevent experimentally induced foot rot in sheep. NZ Vet J 31:54, 1983 45. Skerman TM: Genetic variation and inheritance of susceptibility to foot rot in sheep. In Stewart DJ, Peterson]E, McKern NM, et al (eds): Foot rot in Ruminants. Proc Workshop, Melbourne, 1985. Glebe, NSW, csmo Div Anim Health-Aust Wool Corp, 1986, p 73 46. Skerman TM, Erasmuson SK, Every D: Differentiation of Bacteroides nodosus biotypes and colony variants in relation to their virulence and immune protective properties in sheep. Infect Immunol 32:788, 1981 47. Stewart DF: Treatment and control of foot rot. In Proc ConfVet Officers on Foot-rot and Other Diseases of the Feet of Sheep. Young, New South Wales Department of Agriculture, 1953
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48. Stewart OJ: The role of elastase in the differentiation of Bacteroides nodosus infection in sheep and cattle. Res Vet Sci 27:99, 1979 49. Stewart OJ: Review of foot rot diagnosis and the role of vaccination. Sheep Production and Preventive Medicine, Proc No 67:487, 1983 50. Stewart OJ, Clark BL, Peterson]E, et al: The protection given by pilus and whole cell vaccines of Bacteroides nodosus strain ·198 against ovine foot rot induced by strains of different serogroups. Aust Vet J 62:153, 1985 51. Stewart OJ, Peterson]E, Vaughan JA, et al: The pathogenicity and cultural characteristics of virulent, intermediate, and benign strains of Bacteroides nodosus causing ovine foot rot. Aust Vet J 63:317, 1986 52. Stewart OJ, Peterson ]E, McKern NM, et al: Clinical and laboratory diagnosis of benign, intermediate, and virulent strains of Bacteroides nodosus. In Stewart OJ, et al (eds): Foot rot in Ruminants. Proc Workshop, Melbourne, 1985. Glebe, NSW, csmo Oiv Anim Health-Aust Wool Corp, 1986, p 81 53. Stewart OJ, Elleman TC: A Bacteroides nodosus pili vaccine produced by recombinant ONA for prevention and treatment of foot rot in sheep. Aust Vet J 64:79, 1987 54. Thomas JH: The differential diagnosis of foot rot in sheep. Aust Vet J 38:159, 1962 55. Toussaint Raven E, Cornelisse JL: Transmission of Fusiformis nodosus infection from sheep to cattle. Aust Vet J 46:382, 1970 56. Wilkinson FC, Egerton JR, ~ickson J: Transmission of Fusiformis nodosus infection from sheep to cattle. Aust Vet J 46:382, 1970 Address reprint requests to
Cleon V. Kimberling, BS, OVM, MPH Veterinary Oiagnostic Laboratory College of Veterinary Medicine and Biomedical Sciences Colorado State University Fort Collins, CO 80523
0749-0720/90 $0.00
+ .20
Advances in the Control of Foot Rot in Sheep Cleon V. Kimberling, BS, DVM, MPH, * and Robert P. Ellis, PhDt
Foot rot is a contagious disease of sheep and goats that is transmitted by Bacteroides nodosus. Foot rot may occur in cattle, deer, and possibly other ruminants, although the clinical severity in these animals is much less than in sheep. The disease is characterized by a chronic bacterial infection that is confined to the epidermal tissues of the interdigital skin and horn of the hoof. Contagious ovine foot rot is one of the most limiting diseases of sheep production world-wide. Many producers in the United States have quit sheep production owing to their inability to control foot rot. Australia, the country with the greatest number of sheep in the world, regards foot rot as their most economically important contagious disease of sheep.17 Although tremendous expenditure of research, money, and time has provided new and rewarding control capabilities, the disease remains elusive and extremely difficult to eradicate. DEFINITION AND ECONOMIC IMPACT Ovine contagious foot rot is a complex disease caused by the interaction of two bacteria- Bacteroides nodosus and Fusobacterium necrophorum - and is complicated by macro- and microenvironments, genetics, and micronutrient imbalances that compromise the integumentary and immune systems. Unlike many other diseases, which are caused by individual infectious agents, the collaboration of B. nodosus and F. necrophorum is required to produce clinical disease. F. necrophorum is ubiquitous in the animals' environment and the necessary precursor to the establishment of the invasive B. nodosus. B. nodosus is the essential organism for producing foot rot. Because B. nodosus is a strict anaerobe and is solely dependent on the oxygen-free lesions of the sheep's foot for survival, eradication is possible. From the Colorado State University College of Veterinary Medicine and Biomedical Sciences, Fort Collins, Colorado *Extension Veterinarian, Veterinary Diagnostic Laboratory tProfessor, Veterinary Diagnostic Laboratory and Department of Microbiology Veterinary Clinics o/North America: Food Animal Practice-Vol. 6, No.3, November 1990
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Temperature and moisture play an important role in transmission and invasion of the organism. Therefore, most outbreaks occur during the season of high rainfall, warm temperature, and lush pasture growth. The disease occurs in the temperate climate of all sheep-producing countries in the world. Foot rot was endemic in Britain during the 18th century and was identified in most other major sheep-producing countries during the 19th century.17 The exact economic impact of the disease is impossible to calculate. A monetary figure can be assigned to the additional labor, drug and treatment costs, additional feed, and other expenses, but it is impossible to accurately measure the losses from decreased meat and wool production and increased expenses of other necessary management practices. In a foot rot outbreak involving 1800 Colorado range ewes, 42% were treated at least once. The additional labor, feed, and medication costs were $27.78 for each ewe in the flock. The death loss and loss of production was estimated at an additional $60.00 per head. 19 In an Idaho study, the treatment cost of foot rot in a range flock of 13,000 ewes was calculated to be $4.41 per ewe from 1980 to 1982. Treatment costs represented only 3% of the total expenses of the disease. 3 In an Australian trial, wool-production losses alone in Merino sheep affected with foot rot, compared with unaffected sheep, were estimated at $42.50 per head. 17 In a decision-tree analysis of various treatments and management combinations,41 it was determined that treatment, although costly, is better than no treatment, even when prevalence is very low. The increased profit per ewe in an infected herd was predicted to be $1.79 (at a 10% foot rot prevalence) to $6.45 (30% prevalence) more when sheep were treated with 10% zinc sulfate than when sheep were not treated. Thus, although treatment is expensive, it is theoretically more economic than "living with" the disease. ETIOLOGY AND PATHOGENESIS Etiology B. nodosus and F. necrophomm, pathogenic synergists, cause contagious foot rot. 29 Other organisms often enter the lesions and play an unknown role in the pathogenesis. Although F. necrophomm plays a major role in the pathogenesis,21 the severity of the lesion depends upon the virulence of B. nodosus. B. nodosus is a nonsporing, nonmotile, noncapsulating, granular, gram-negative, anaerobic bacillus with bulbous ends. The pili on the cell membrane are associated with virulence and antigenicity. 22,27,32,50,51 There are more than 22 B. nodosus serogroups, each exhibiting varying degrees of virulence. 49 Pathogenesis Beveridge 2 pioneered the work on the etiologic agents, pathogenesis, and epidemiology of contagious foot rot. During his investigations, he observed that the organisms currently classified as B. nodosus and F. necrophorum were synergistic in producing virulent foot rot. He also observed that foot rot of greater severity was more consistently produced when Spirochaeta penortha was present. More recent studies by Hine 28 have shown that apart from B. nodosus and F. necrophomm, a filamentous rod-shaped bacterium is also associated with F. necrophomm in the tissues and appears to have the ability to penetrate keratinized tissues directly. The growth characteristics are apparently consistent with those of the motile organism described by Beveridge. The findings of these workers indicate that foot rot is a complex disease caused by the synergistic actions of F. necrophomm and other organisms limited by the essential transmitting and virulence agent B. nodosus. Edgerton et
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al lS concluded that following colonization of macerated interdigital skin, F. necrophorum facilitates infection with B. nodosus, probably by inducing hyperkeratosis and parakeratosis. This results in crevices where anaerobic bacteria can survive and multiply. F. necrophorum, because of its invasiveness and elaboration of exotoxin, is responsible for most of the inflammation and initiation of tissue damage. B. nodosus has minimal inflammatory capabilities but initiates the invasion and extension of the lesion into the hoof matrix. B. nodosus is able to persist in lesions for long periods, thereby sustaining the infection. It also produces a heat-stable soluble factor that enhances the infectivity and invasiveness of F. necrophorum, a normal inhabitant of the sheep intestinal flora that is ubiquitous in the environment. The pathogenesis of contagious foot rot begins with transmission of B. nodosus from the environment to macerated or scald-affected interdigital skin. At the skin-horn junction near the axial bulbar notches, F. necrophorum and possibly other unidentified organisms begin the disease process by colonizing the moist epidermal surface; only then does B. nodosus, as the second step, adhere to the host tissue, colonize the sites on the feet that have lowered oxygen tension, penetrate the tissue and, owing to the pili, colonize the epidermis of the hoof. By action of its powerful keratinolytic protease, B. nodosus liquefies the cells of the stratum granulosum and stratum spinosum and thus cleaves the cells and separates the horn corium from the basal epithelium and derma. 29 The ensuing waves of F. necrophorum account for the strong and damaging inflammation. The degeneration, detachment, and liquefactive digestion of partially keratinized cells of the stratum lucidum and stratum spinosum, as well as formation of fissures, sinuses, and necrotic foci in the keratinized horn, appear to be directly related to the presence of B. nodosus. The ability of B. nodosus to maintain itself for long periods in apparently healed lesions and the recurrent waves of F. necrophorum associated with suitable microenvironmental changes probably account for the recurrent episodes of severe clinical foot rot. Host Susceptibility Parker et aP7 in the United States and Skerman45 in Australia have shown that resistance to foot rot is a genetically heritable trait in selected Targhee and Romney sires. Australian workers 14,17,45 reported variability between breeds, with the British-breed sheep being more resistant than the Merino. Age also appears to be a factor. As age increases, resistance apparently decreases. There is a wide spectrum of resistance within any sheep population; some individuals withstand repeated challenges, whereas others succumb to acute infection and may heal spontaneously or become clinically infected carriers. Transmission Infective material is transferred directly from an exposed lesion onto soil, thereby providing a contaminated environment for the feet of other sheep. Exposure of susceptible sheep is provided by the nature of sheep to congregate in groups during the heat of the day, trail single file along paths to and from water, or use a common watering or feeding area. B. nodosv~, because it is anaerobic and oxygen sensitive, dies rapidly once it is away from the lesion of its host. The organism lives no longer than 4 to 5 days in contaminated material. 31 It is totally host-dependent for multiplication and long-term survival. Mechanical transmission to other farms or ranches on various fomites such as boots, vehicle tires, feet of animals other than sheep, and so on is possible but improbable. Owing to the highly contagious nature of the organism, infected sheep are the most probable mode of spread from farm to farm. Mechanical
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transmission via instruments used in paring hooves is possible; therefore, they should be disinfected between sheep. I Any management practices that tend to concentrate sheep into small areas such as high stocking rates on irrigated pastures, access to streams or watering facilities, feedlots, common trails, and so on increase the risk and likelihood of transmission. Predisposing Environmental Factors Conditions of high moisture, warm temperatures, lush pasture growth, and a susceptible host, together with a source of infection, favor outbreaks of the disease. In temperate climates, the spread and outbreaks of foot rot are usually associated with the rainy season and a mean ambient temperature above 10°C, or 50°F. There are areas of the northwestern and southeastern United States that remain ideal for foot rot spread throughout the year, whereas foot rot is a seasonal disease, maintained in the feet of chronically infected animals, in the midwest and northeast. The western mountain and intermountain range areas, although extremely arid, experience severe localized outbreaks owing to environmental niches within these vast expanses that are moist and have lust plant growth, which tends to attract concentrations of animals to those habitats. Some range operators may use common trails and working facilities and overlap on grazing permits. Stray animals may enter other Hocks because, owing to lameness, the strays were unable to keep up with the parent Hock. The extremely contagious characteristics of B. nodosus play an important role in the transmission of foot rot from sheep to sheep within the Hock or between Hocks. Unfortunately, most foot rot is introduced through the purchase of infected animals. Under ideal transmission conditions, 70% or more of an unvaccinated Hock will develop foot rot in an outbreak if no prophylactic precautions are taken. 15 Soil moisture appears to be the limiting factor in transmission. Beveridge l noted that foot rot was much more prevalent on improved fertilized pasture with lush growth containing clover than on natural pasture of lighter carrying capacity. The improved and irrigated pastures create an ideal microenvironment for the spread of foot rot - first, by concentrating animals and, second, by allowing better retention of surface moisture. Transmission of foot rot ceases as the total environment dries out, with the consequent dehydration of the interdigital skin, although there may be sufficient moisture for continued plant growth. 25 As noted previously, small niches of moist to muddy soils, such as that found at waterholes, stream crossings, and water troughs, also serve as very successful areas for transmission. Reservoir of Infection After foot rot occurs, there is chronic disease, inapparent infection, or complete recovery. An individual sheep that completely recovers does not serve as a source of infection for other susceptible sheep. In any outbreak, natural healing is a normal feature, with a variable proportion of the infected sheep remaining chronically or inapparently infected. Chronically infected animals do not pose a particular threat, because they can be easily identified and eliminated, whereas the inapparent or symptomless carrier constitutes a risk to the remainder of the population. In one type of inapparent state, the infection may be in small foci under healthy horn, which can only be identified by careful paring. Some of these cases can be identified by a slightly misshapen hoof. If undetected, these pose a potential threat of reinfection if the sequestered infection breaks out to the surface. Benign strains may be more subtle in their clinical manifestation and, therefore, more difficult to detect and eliminate, with the inapparent carrier being the reservoir for reinfection when conditions become ideal.
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In Australia, several benign strains of B. nodosus have been isolated from farmed red deer and cattle. In passage to sheep, these strains have caused benign foot rot. 30,46,48,55,56 Natural transmission of virulent B. nodosus from sheep to cattle has not been successful. 30 Australian workers consider it highly probable that cattle are a reservoir for benign foot rot of sheep,40 but in relation to virulent foot rot it is unlikely that cattle constitute a major risk to sheep.40 Because goats can be infected with virulent and benign strains, they can be a potential reservoir. 5,52 In the United States, deer, elk, bighorn sheep, and goats have not been investigated, and their role as reservoirs is unknown. In endemic areas, sheep remain the most likely carriers. Clinical Signs The clinical signs observed in sheep affected with foot rot depend on a variety of factors, including the virulence of the organism, the climatic environment, the health or trauma to the interdigital skin, and a number of host factors. Although three types of foot rot are described in Australian literature 19,54 (virulent, intermediate, and benign), there are basically two clinically recognizable forms of foot rot in sheep: virulent and benign. InHammation of the interdigital skin is seen with both forms. Virulent foot rot is characterized by extensive separation, which commences at the heel, extends to the sole and toe, and frequently involves separation of the abaxial wall, with the formation of a distinctive, foul-smelling, necrotic exudate. Benign foot rot (a form of scald) is characterized by occasional separation of the horn of the heel bulbs and posterior sole region, but there is a limited accumulation of necrotic material under the separated horn. 12,54 Benign foot rot is further characterized by causing only a mild lameness that rapidly regresses following topical treatment or after the onset of dry environmental conditions. 12 In comparison, virulent foot rot causes severe lameness that persists and requires intensive treatment to alleviate the symptoms. In any severe outbreak of virulent foot rot, a wide spectrum of clinical involvement may be seen. In a Colorado study, Ellis et al 19 developed a scoring system of 0 - 3 for assessing severity, which correlates closely with the virulent, intermediate, and benign system. A score of 0 indicates no foot rot, 1 indicates an initial lesion of the interdigital skin between the toes or at the heel, 2 indicates the lesion has advanced with some underrunning of the sole, and 3 indicates there is underrunning of the sole and abaxial wall with a foul-smelling exudate. It is possible to see all four conditions on one individual. CONTROL AND ERADICATION Contagious foot rot in sheep causes reduced weight gain and wool yield (and death), which results in economic losses to sheep producers world-wide. Many treatment regimens and preventive measures for this disease have been proposed. Before deciding which method of prevention or treatment is most appropriate for a given Hock situation, sheep owners and veterinarians should consider the cost and the likely economic benefit of the various treatments and control procedures. 41 Because foot rot is a relatively superficial bacterial infection localized in the zone between the keratinized horn and the avascular living epidermal tissues of the hoof and still accessible to substances diffusing from the blood stream, several therapeutic options are available. Surgical paring of the hoof to expose the lesions followed with topically applied antibacterial agents, although labor intensive and time-consuming, is an effective means of treatment. To be effective, the surgical preparation of the
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foot is very important. Each foot must be thoroughly examined and meticulously pared. The full extent of the infection must be exposed by removing all underrun sole and wall covering the lesion. 35 Proper and adequate restraint are essential to an effective paring procedure. A simple manual tip-over restraining device can be built, or more sophisticated, commercially available restraining devices can be used. Whatever the device, it is essential that all feet are easily accessible. To ensure adequate and proper paring, a good set of hand shears with good blades and a sharp paring knife are essential. Hemorrhage is undesirable because it may mask the operative field and interfere with the action of the topical agent. It is better not to be too conservative, because insufficient paring may leave pockets of infection. 39 Paring should be done from heel to toe to minimize bleeding. 39 Following paring, topical bactericidal agents are applied to the exposed diseased tissue. Quaternary ammonium antiseptic solutions, iodophor antiseptic solutions, iodine, or 10% zinc sulfate in water give excellent results. 6 Cross6 showed that a 10% zinc sulfate solution was more effective than a 10% formalin or a 10% copper sulfate solution. For best results, the sheep should be kept on a dry surface (concrete or board) for at least 1 hour following topical treatment. 2,38,47 Footbathing When large numbers of sheep are involved, footbathing is a practical alternative to individual treatment. Over the years, copper sulfate and formalin have been the standard materials used in footbaths. More recently, a 10% to 20% zinc sulfate solution with 2% sodium lauryl sulfate has proved as effective as formalin or copper sulfate. Footbaths containing zinc sulfate have been shown to be effective, safe, practical, and economic. Cross and Parker8 demonstrated that daily footbathing in 10% zinc sulfate for 30 days, without paring, greatly reduced the number of clinical cases. Malecki and McCausland33,34 showed that, in vitro, the anionic surfactant sodium lauryl sulfate increased the penetration of zinc sulfate into the hoof approximately sixfold, whereas formaldehyde did not penetrate at all. Bulgin et al 4 found that footbathing in 10% zinc sulfate (containing 0.2% heavy-duty laundry detergent with nonionic surfactants) for 1 hour at IO-day intervals was an effective treatment of chronic cases without the necessity of foot paring. A 10% zinc sulfate - surfactant solution with a 10 to 30 minute soak at 5-day intervals appears to be ideal for curing interdigital and benign cases of foot rot. The zinc sulfate solution can be prepared using fertilizer-grade zinc sulfate. The rough formulation of a 10% ZnS04 solution is BIb ZnS04/10 gal of water. Fertilizer grade ZnS04 is usually 35.5% or 22.7% zinc. Therefore, to obtain a 10% solution, 22.5 pounds of 35.5% ZnS04 or 35 pounds of 22.7% ZnS04 should be used per 10 gallons of water . Warm water greatly enhances the solubility of the ZnS04' A satisfactory wetting agent such as sodium lauryl sulfate should be added at a 0.2% vol:vol concentration (approximately two thirds of a cup per 20 gallons of water). Although this treatment has a high curative rate on severe and chronic cases, the effectiveness is improved with paring. 4,35,36 In some cases, improper paring can be detrimental to the cure rate. Of the three products currently being used (zinc sulfate, copper sulfate, and formalin) for footbath solutions, zinc sulfate has no irritating fumes, is less toxic, does not stain the wool, and is nonirritating to the skin. Parenteral Antibiotic Therapy Numerous trials have been conducted on parenteral antibiotic treatment of contagious foot rot. In a study ~onducted by Gradin and Schmitz,24 it was found
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that penicillin was the most effective of a wide range of antimicrobials tested, including the newer antibiotics cephalosporin and clindamycin. Harris 26 observed that when using parenteral antibiotics the cure rate was improved and subsequent assessment was easier and more accurate if the sheeps' feet were thoroughly pared. In wet conditions, better results were obtained if sheep were housed on slotted Hoors in a dry environment for 24 hours after treatment. 11 An interdigital subcutaneous injection of penicillin-streptomycin was no more effective than the intramuscular route. 6 From all of the trials and field observations conducted, it appears that parenteral antibiotics have a fairly high cure rate and have the added advantage of reaching the undetected sequestered lesion. The disadvantage of mass parenteral antibiotic therapy is the tremendous expense without complete cure or eradication. This method of therapy is probably suited for select individuals for which careful hoof paring and close observation is possible. There is also the potential human health hazard of drug-resistant organisms and food safety. The report by Demertzis and Mills, 9 that healing of cases of bovine infectious pododermatitis in bull calves could be attributed to a daily intake of zinc as a drench, stimulated investigations into oral zinc therapy for prevention and cure of ovine contagious foot rot. A wide spectrum of dosage ranges was fed over periods extending to 6 months. It was concluded from these studies that oral zinc was of no practical benefit in reducing the prevalence or severity of B. nodostlS infections in treated animals and did not enhance the resistance of sheep to foot rot. 6 ,7,9,10,16,24,44 Immunization Immunization can provide the most efficient and cost-effective control of foot rot provided an effective vaccine is used. Following the release of Footvax (Coopers Animal Health Australia, formerly ICI Australia Pty) in 1981 and Pro-vac (Coopers Animal Health Australia, formerly Wellcome Australia Pty) in 1982, United States researchers in Idaho, California, and Colorado conducted efficacy trials. 3 ,19,23 To license a commercial vaccine in Australia, the cure rate must be at least 65% with a protection rate of 70% at 6 and 12 weeks, respectively, after vaccination. With cure rates, there must be at least 20% affected initially, and for protection rates, 30% of infected sheep in the unvaccinated control group must be infected at the time protection is measured. Although the vaccine provides prophylactic and preventive benefits, it does not provide complete protection and must be used with other management practices of trimming, foot soaking, and vigorous culling if foot rot is to be eliminated from a flock. Besides being expensive, the vaccine produces granulomas and abscesses at the injection site (30%-70%), which usually resolve in a few weeks and are of only cosmetic importance. In the continuation of the Colorado study, where vaccination was carried out annually at 4 to 6 weeks prior to the period of highest transmission, the incidence was reduced from an initial infection rate of 15% in April 1985 to 0.2% in July 1986. The reduction was greatly enhanced by paring, footbathing, and culling. Failure to cull a few chronically infected ewes resulted in an outbreak in 1987 involving 15% of the flock. Recently (June 1989), with increased paring and culling, the incidence in this flock is back down to 2.4% (Ellis and Kimberling, unpublished results). These observations further indicate that vaccination is only one element of a control program. Ideally, it should be possible to effectively control foot rot using vaccines, without the need of the labor-intensive operations of foot paring and footbathing. Research is currently being conducted in the United States and Australia on recombinant DNA vaccines. The initial trials are extremely promising, with increased efficacy and reduced production costs. 18,53
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Control and Eradication With our current knowledge, it is safe to say that foot rot can be eradicated from a population of sheep. A successful program is dependent on a number of factors, the most critical being the commitment and understanding of contagious foot rot by management and all persons involved with the operation. This involves a thorough understanding of the disease and the highly contagious properties of B. nodosus. All diseases, including contagious foot rot, have similar steps in the infectious process. Understanding the individual characteristics of the organism, how it survives in the host, how it escapes from the host, its survivability in the environment, the properties of transmission, and the susceptibility factors of the new host are all integral in control of foot rot. In contagious foot rot of sheep, we know that B. nodosus is the limiting organism for infection. It has the capability of surviving in walled-off lesions in the misshapen hoof for extended periods of time and the ability to change from a latent, inapparent infection to an acute, virulent infection when the microenvironment is favorable. Outside the host, survival is short (4 to 7 days) and dependent on a mean ambient temperature of 50°F (10°C) with adequate humidity and moisture. The organism is susceptible to penicillin via parenteral injections or can be killed by direct contact with zinc sulfate, copper sulfate, or formalin. The more than 22 serotypes of B. nodosus have different invasive, virulence, and immunogenic properties. The primary reservoir is sheep, with goats, cattle, and deer being infected but playing a minor role or no role whatsoever in the spread of the disease. There are genetic differences between breeds and within breeds, with the Merino being highly susceptible and the Romney exhibiting some degree of resistance. Selected sires have been identified that produce resistant offspring. The resistance of the host can definitely be increased with available vaccines. None of the available vaccines will give absolute protection, but with paring, footbathing, and culling, they will enhance a control and eradication program. New methods of vaccine development and delivery are encouraging and should enhance our ability to control and eradicate foot rot. Taking the known facts about the organism plus the interaction of the environment and the host, we can outline a suitable plan to prevent, control, or eradicate the disease. The plan must be individually tailored for each enterprise, because no two operations have identical environments, facilities, or management. An assessment of prevalence and the economic impact on production will determine if control or eradication is the most cost-effective program. The basic steps are the same regardless of the plan. SUMMARY All cases of foot rot, whether acute, chronic, benign, or inapparent, must be identified. If the outbreak is severe and production losses warrant, each foot of each animal must be examined thoroughly. Proper handling facilities and equipment, adequate light, and dry working conditions are needed to properly examine each foot. Infected sheep must be separated from the clean Hock. Following extensive treatment, these animals must be diagnosed as free from the disease before returning to the clean Hock. Animals that do not respond must be culled from the Hock. Although copper sulfate and formalin are effective materials for footbathing, zinc sulfate is equally effective and does not irritate the skin, eyes, or lungs as does formalin, or stain the wool as does copper sulfate. A 10% zinc sulfate
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solution with a nonionic surfactant is an effective footbathing or foot soaking solution. The cure rate is improved by a thorough foot paring and a foot soak of at least 30 minutes. A number of treatment options along with formulations are outlined in the 1988 edition of the Sheep Production Handbook of the Sheep Industries Development Program, Inc, 6911 Yosemite, Englewood, CO 80112.
REFERENCES
1. Beveridge WIB: Foot-rot in sheep: A transmissible disease due to infection with Fusifonnis nodosus. Studies on its cause, epidemiology, and control. J Counc Sci Ind Res, Bull 140:14, 1941 2. Beveridge WIB: Bacterial diseases of cattle, sheep, and goats. Canberra, Aust Govt Pub Ser, 108:178, 1983 3. Bulgin M, Lincoln SD, Lane VM, et al: Evaluating an ovine foot-rot vaccine. Vet Med 80:105, 1985 4. Bulgin MS, Lincoln SD, Lane VM, et al: Comparison of treatment methods for the control of contagious ovine foot rot. J Am Vet Med Assoc 189:194, 1986 5. Claxton PD, O'Grady KC: Foot rot in goats and characterization of caprine isolates of Bacterioides nodosus. In Stewart DJ, Peterson JE, McKern NM, et al (eds): Foot rot in Ruminants. Proc Workshop, Melbourne, 1985. Glebe, NSW, csmo Div Anim Health/Aust Wool Corp, 1986, p 119 6. Cross RF: Response of sheep to various topical, oral, and parenteral treatments for foot rot. J Am Vet Med Assoc 173:1569, 1978 7. Cross RF, Parker CF: Oral administration of zinc sulfate for control of ovine foot rot. J Am Vet Med Assoc 178:704, 1981 8. Cross RF, Parker CF: Zinc sulfate footbath for control of ovine foot rot. J Am Vet Med Assoc 178:706, 1981 9. Demertzis PN, Mills CF: Oral zinc therapy in the control of infectious pododermatitis in young bulls. Vet Rec 93:219, 1973 10. Demertzis PN, Spais AG, Papasteriadis AA: Zinc therapy in the control of foot rot in sheep. Vet Med Rev 1:101, 1978 11. Egerton JR, Parsons on 1M, Graham NPH: Parenteral chemotherapy of ovine foot rot. Aust Vet J 44:284, 1968 12. Egerton JR, Parsonson 1M: Benign foot rot-a specific interdigital dermatitis of sheep associated with infection by less proteolytic strains of Fusifonnis nodosus. Aust Vet J 45:345, 1969 13. Egerton JR, Roberts DS, Parsonson 1M: The aetiology and pathogenesis of ovine foot rot. I. A histologic study of the bacterial invasion. J Comp Pathol 79:207, 1969 14. Egerton JR, Morgan m: Foot rot in vaccinated and unvaccinated sheep. I. Incidence, severity, and duration of infection. Vet Rec 91:447, 1972 15. Egerton JR, et al: Onset and remission of ovine foot rot. Aust Vet J 60:334, 1983 16. Egerton JR. Laing EA, Mulley RC: Failure of oral zinc therapy to alleviate Bacteroides nodosus infection in cattle and sheep. Aust Vet J 62:85, 1985 17. Egerton JR, Yong WK, RiHkin GG: Foot Rot and Foot Abscess of Ruminants. Boca Raton, Florida, CRC Press, 1989, p 7 18. Egerton JR, et al: Protection of sheep against foot rot with a recombinant DNA-based fimbrial vaccine. Vet MicrobioI14:393, 1987 19. Ellis RP, et al: The efficacy of Footvax in the control of foot rot. Sheep Industry Development Res Dig, Winter 1986, p 7 20. Emery DL, Stewart DJ, Clark BL: The structural integrity of pili from Bacteroides nodosus is required to elicit protective immunity against foot rot in sheep. Aust Vet J 61:237, 1984 21. Emery DL, et al: Cultural characteristics and virulence of strains of Fusobacterium necrophorum isolated from the feet of cattle and sheep. Aust Vet J 62:43, 1985 22. Every D, Skerman TM: Surface structures of Bacteroides nodosus in relation to virulence and immunoprotection of sheep. J Gen Microb 129:225, 1983
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23. Glenn J, Carpenter TE, Hird DW: A field trial to assess the therapeutic and prophylactic effect of a foot rot vaccine in sheep. J Am Vet Med Assoc 187:1009, 1985 24. Gradin JL, Schmitz JA: Susceptibility of Bacteroides nodosus to various antimicrobial agents. J Am Vet Med Assoc 183:434, 1983 25. Graham NPH, Egerton JR: Pathogenesis of ovine foot rot: The role of some environmental factors. Aust Vet J 44:235, 1968 26. Harris DJ: Field observations on parenteral antibiotic treatment of ovine foot rot. Aust Vet J 44:284, 1968 27. Hindmarsh F, Fraser J: Serogroups of Bacteroides nodosus isolated from ovine foot rot in Britain. Vet Rec 116:187, 1985 28. Hine PM: Ovine Foot rot: Histopathology of a synergistic disease. In Hill MJ (ed): Models of Anaerobic Infection. The Hague, Martinus Nijhoff, 1984, p 85 29. Kimberling CV: Jensen and Swift's Diseases of Sheep. Philadelphia, Lea & Febiger, 1988, p 317 30. Laing EA, Egerton JR: The occurrence, prevalence, and transmission of Bacteroides nodosus infection in cattle. Res Vet Sci 24:300, 1978 31. Laing EA, Egerton JR: Some aspects of B. nodosus infection in cattle. In Ovine Foot rot, Rep Workshop, University of Sydney, May 3, 1981, p 195 32. Lee SW, Alexander B, McGowan B: Purification, characterization, and serologic characteristics of Bacteroides nodosus pili and use of a purified pili vaccine in sheep. Am J Vet Res 44:1676, 1983 33. Malecki JC, McCausland IP: Improvement of topical chemotherapy of ovine foot rot by increasing the penetration of therapeutic agents. In Ovine Foot rot, Rep Workshop, University of Sydney, 1981, p 165 34. Malecki JC, McCausland IP: In vitro penetration and absorption of chemicals into the ovine hoof. Res Vet Sci 33:192, 1982 35. Malecki JC, McCausland IP, Lambell R: A new topical treatment for foot rot. Proceedings No. 67, Sheep Production and Preventive Medicine, University of Sydney, 1983, p 63 36. Malecki JC, Coffey L: Effectiveness of treatment programs based on footbathing with a zinc sulphate formulation for virulent Bacteroides nodosus infection in sheep. In Stewart DJ, Peterson ]E, McKern NM, et al (eds): Foot Rot in Ruminants. Proc Workshop, Melbourne, 1985. Glebe, NSW, csmo Div Anim Health-Aust Wool Corp, 1986 37. Parker CF, Cross RF, Hamilton KL: Genetic resistance to foot rot in sheep. Annu Proc Sheep Vet Soc 9:16, 1985 38. Penny RHC: The topical application of 10% chloramphenicol in spirit in the treatment of foot rot in sheep. Br Vet J 11:125, 1985 39. Pryor WJ: The treatment of contagious foot rot in sheep. Aust Vet J 30:385, 1954 40. Richards RB, Depiazzi LJ, Edwards JR, et al: Isolation and characterization of Bacteriodes nodosus from foot lesions of cattle in western Australia. Aust Vet J 56:517, 1980 41. Salman MD, Dargatz DA, Kimberling CV, et al: An economic evaluation of various treatments for contagious foot rot in sheep, using decision analysis. J Am Vet Med Assoc 193:195, 1988 42. Sheep Industry Development Handbook, Health Chapter. Englewood, CO, American Sheep Industry Association, 1988 43. Sinclair AN: Studies on contagious foot rot of sheep. Aust Vet J 33:202, 1957 44. Skerman TM, Millar KR, Sheppard AD, et al: Failure of orally administered zinc to prevent experimentally induced foot rot in sheep. NZ Vet J 31:54, 1983 45. Skerman TM: Genetic variation and inheritance of susceptibility to foot rot in sheep. In Stewart DJ, Peterson]E, McKern NM, et al (eds): Foot rot in Ruminants. Proc Workshop, Melbourne, 1985. Glebe, NSW, csmo Div Anim Health-Aust Wool Corp, 1986, p 73 46. Skerman TM, Erasmuson SK, Every D: Differentiation of Bacteroides nodosus biotypes and colony variants in relation to their virulence and immune protective properties in sheep. Infect Immunol 32:788, 1981 47. Stewart DF: Treatment and control of foot rot. In Proc ConfVet Officers on Foot-rot and Other Diseases of the Feet of Sheep. Young, New South Wales Department of Agriculture, 1953
ADVANCES IN THE CONTROL OF FOOT ROT IN SHEEP
681
48. Stewart OJ: The role of elastase in the differentiation of Bacteroides nodosus infection in sheep and cattle. Res Vet Sci 27:99, 1979 49. Stewart OJ: Review of foot rot diagnosis and the role of vaccination. Sheep Production and Preventive Medicine, Proc No 67:487, 1983 50. Stewart OJ, Clark BL, Peterson]E, et al: The protection given by pilus and whole cell vaccines of Bacteroides nodosus strain ·198 against ovine foot rot induced by strains of different serogroups. Aust Vet J 62:153, 1985 51. Stewart OJ, Peterson]E, Vaughan JA, et al: The pathogenicity and cultural characteristics of virulent, intermediate, and benign strains of Bacteroides nodosus causing ovine foot rot. Aust Vet J 63:317, 1986 52. Stewart OJ, Peterson ]E, McKern NM, et al: Clinical and laboratory diagnosis of benign, intermediate, and virulent strains of Bacteroides nodosus. In Stewart OJ, et al (eds): Foot rot in Ruminants. Proc Workshop, Melbourne, 1985. Glebe, NSW, csmo Oiv Anim Health-Aust Wool Corp, 1986, p 81 53. Stewart OJ, Elleman TC: A Bacteroides nodosus pili vaccine produced by recombinant ONA for prevention and treatment of foot rot in sheep. Aust Vet J 64:79, 1987 54. Thomas JH: The differential diagnosis of foot rot in sheep. Aust Vet J 38:159, 1962 55. Toussaint Raven E, Cornelisse JL: Transmission of Fusiformis nodosus infection from sheep to cattle. Aust Vet J 46:382, 1970 56. Wilkinson FC, Egerton JR, ~ickson J: Transmission of Fusiformis nodosus infection from sheep to cattle. Aust Vet J 46:382, 1970 Address reprint requests to
Cleon V. Kimberling, BS, OVM, MPH Veterinary Oiagnostic Laboratory College of Veterinary Medicine and Biomedical Sciences Colorado State University Fort Collins, CO 80523