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Changes in the Sheep Industry in the United States: Making the Transition from Tradition 3 Sheep Health Issues Maintaining the health of a flock is imperative for a successful sheep operation because disease imposes both apparent as well as hidden costs on the operation. Obvious expenses include the price of treatments and death loss. Hidden costs can be attributed to disease-related production inefficiencies. For example, a ewe that is lame or one that suffers from ovine progressive pneumonia (OPP) will produce less milk than her genetics or nutrition should allow and, therefore, may raise lambs with a reduced rate of gain. There are little or no data, however, on the economic impacts or the true prevalence of most of the disease conditions affecting sheep in United States. The lack of this information makes it quite difficult to make decisions regarding the allocation of resources as well as the determination of research and policy priorities. Some of the more common costs associated with ill or unthrifty sheep include but may not be limited to: Treatment; Mortality; Premature culling; Lower number of live lambs born as a result of (1) failure of the ram to settle ewes, (2) reduced conception rates, (3) failure to carry lambs to term, and (4) failure to give birth to live lambs; Reduced birth weights; Weak lambs (little or no colostrum); Reduced rate of gain either due to poor milk production by the ewe or poor health of the lamb;
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition Disease that results in wool loss or lower quality wool; and Labor costs associated with treatment. Maintaining the health of the national flock has even broader implications than for any given individual flock. An introduction of a foreign animal disease or an endemic disease that mutates may result in large-scale repercussions such as a food safety event that could result in human illness and decreased consumer confidence. In the past decade, > 70 percent of the emerging diseases have been zoonotic (Woolhouse and Gowtage-Sequeria, 2005). The U.S. sheep industry has been fortunate to avoid a significant crisis resulting from a highly contagious or zoonotic disease outbreak. To prevent complacency, the industry as a whole will need to systematically review worldwide conditions and disease reports as well as suspicions of diseases mutating to a more virulent strain. One of the greatest vulnerabilities is the risk of introducing a foreign animal disease. When introduced into a native population, foreign animal diseases may spread rapidly because the animals have no immunity to the disease. In many cases, the outbreaks result in a high death losses and/or severe production losses. To illustrate that the cost of prevention is usually much less expensive than control or elimination, the World Organization for Animal Health (OIE) commissioned a study to compare the cost of preparedness and prevention versus the cost of control for avian influenza. Even without considering the indirect financial impacts, the benefits of prevention far outweighed the potential outbreak costs and losses (Agra CEAS Consulting, 2007). The intent of this chapter is to examine broad issues regarding health and how they may impact the economic viability of the sheep industry as a whole, as well as individual sheep operations. The chapter is not intended to serve as a comprehensive review of sheep diseases. Certain diseases are highlighted to illustrate different points. A detailed review of scrapie is included because it is the only sheep disease that has had a congressionally funded control program in place for over 50 years. MANAGEMENT PRACTICES REGARDING HEALTH Sound flock health management practices are the key to disease prevention and control. While it is important to have vaccination and treatment programs for specific diseases, a holistic approach founded on prevention can be the most effective tool for maintaining a healthy flock. This in turn increases productivity. The basic management tools include: Biosecurity, including maintaining a closed flock or restricting the number and source of replacements; Recordkeeping, including animal identification;
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition Technical resources; and Availability of effective vaccines and treatments. Biosecurity and Replacement Practices Diseases gain entry into and spread within flocks by various routes. Most commonly, they are brought in by the introduction of new animals or by animal contact at points of concentration such as shows, sales, fairs, and sale barns. Disease can also be spread by vectors that include visitors, equipment, feed, and insects. Good hygiene and biosecurity measures are important methods of preventing the spread of disease into and within a flock. Although there are costs associated with biosecurity measures, they have the potential to halt the entry of pathogens that may result in disease. As stated previously, the costs associated with disease are both direct (treatment and mortality losses) and indirect (production losses) and usually are higher than the expense of prevention. Biosecurity refers to measures taken to keep diseases out of populations, herds, or groups of animals or to limit the spread of diseases. Successful biosecurity measures must address isolation of new animals brought to the farm; isolation of sick animals; regulation of the movement of people, animals, and equipment; correct use of feed; and procedures for cleaning and disinfecting facilities. The responsibility for a successful biosecurity program falls on the owner (European Community, 2007). The American Sheep Industry Association (ASI) has a fact sheet on biosecurity that provides useful advice.1 The 2001 National Animal Health Monitoring System (NAHMS) study (USDA, 2002) found that more than one-half of the sheep operations with 100 or more head added replacements from the outside in 2000. This was also true for approximately 25 percent of operations with 1–24 sheep and close to 40 percent of the operations with 25–99 head. Approximately 80 percent of all operations added sheep in the last 9 years (USDA, 2003a). New replacements from other flocks pose a risk of introducing a disease into an existing flock. Certain precautions may be taken to minimize this risk. Effective prevention measures may include obtaining a complete history of the flock of origin, testing for certain diseases prior to and after movement, isolation and quarantine on the new farm, vaccination, treatments such as medicated foot baths, and deworming. When introducing/ purchasing animals from another farm a good practice is to investigate the health status of the flock of origin. This inquiry should include a discussion 1 http://www.sheepusa.org/index.phtml?page=site/text&nav_id=3c081c2af5f98f1a054911d06824094f.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition with the producer about biosecurity practices, as well as a review of vaccination and testing programs, veterinary visits, and laboratory reports. Although quarantine is an effective way to monitor for and prevent disease introduction, only 33.9 percent of operations accounting for 16.4 percent of new additions administer any type of quarantine prior to commingling new animals with the existing flock. Contact with other sheep during shows, exhibitions, breeding, grazing, and other encounters also poses a risk of disease transmission. Over 50 percent of operations report such contacts, yet less than 30 percent made an attempt to decrease nose-to-nose contact (USDA, 2003a). On most operations, the major treatments performed on the new additions either prior to or upon arrival include deworming (75.2 percent) and vaccination (61.8 percent). A larger percentage of operations performed these two treatments after arrival than before movement. Another effective method of keeping certain diseases out of flocks is to test for diseases prior to an animal leaving a flock and then retest again in quarantine. This does not appear to be a common practice. Only 6.3 percent of operations test for OPP and 3.4 percent for Johne’s disease prior to or upon arrival into the new flock (USDA, 2002). Visitors who borrow equipment, feed, rendering, and other service-related vehicles can also bring disease agents onto a farm. This is especially true with highly contagious diseases such as foot and mouth disease (FMD). Of operations that allowed visitors, only 22.6 percent had any biosecurity requirements for visitors. A proactive management practice is to prevent introduction of disease into a flock rather than reacting to an introduction or outbreak of disease. Prevention is also the safest and least costly method of protection. A plan of prevention requires each farm or ranch operator to carefully evaluate their management practices in order to identify specific practices that could present potential risks in their production unit and incorporate the common sense biosecurity practices necessary to reduce those risks. Biosecurity management plans are intended to minimize the factors that increase the risk of disease transmission into and within flocks and maximize the factors that decrease disease. The existing data suggest that certain producer behaviors and lack of effective disease management practices increase the vulnerability of many sheep operations to disease (USDA, 2003b). There are a number of important endemic diseases or disease conditions that can enter a flock unless adequate biosecurity measures are in place. These are described in the following subsections:
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition Infectious Foot Rot Infectious foot rot can quickly become a chronic problem. It is difficult to eliminate, requiring time, labor, and financial resources. Foot rot can be introduced by adding sheep from any source, borrowing rams for breeding, sharing infected pastures, sharing common holding areas such as at sales and shows, and sharing common hauling or shearing trailers. Warmth and moisture, which are conducive environmental conditions for the transmission of foot rot, can lead to a large proportion of a flock becoming infected within 1–2 weeks. Foot rot in sheep has two forms, benign and virulent. The virulent form may be quite severe, causing an animal to limp or be unwilling to place weight on one foot. If more than one foot is affected an animal may graze on its knees or not get up at all. Economic losses may be considerable and consist of treatment costs for labor, drugs, vaccines, and equipment; decreased flock productivity (poor growth rates, reduced wool growth and poor wool quality and reduced fertility); and loss of sales. Foot rot is the result of the action of two bacteria. Fusobacteria necrophorum, which is present in the environment, assists Dichelobacter (formerly Bacteroides) nodosus, the causal agent in its quest to invade the hoof. D. nodosus does not survive in the environment for more than a few days to 2 weeks. It can, however, persist in the feet of infected sheep for many years even under dry conditions. Foot baths, parenteral antibiotics, topical treatments, vaccines, trimming of the feet, and rigorous culling, as well as determination and dedication may be required to eliminate foot rot from a flock. Some producers opt to depopulate and start over. Prevention is the best option (Seaman and Evers, 2006; Radostits et al., 2007). Ovine Progressive Pneumonia (OPP) Ovine progressive pneumonia (OPP), which is also known as Maedi-Visna in Europe, is caused by an ovine lentivirus that induces a persistent infection in sheep and may result in lymphoproliferative changes in the lung, mammary gland, brain, and/or joints. Because of the nature of the virus, the animal never develops complete immunity and fails to completely eliminate the virus. Lambs may become infected at birth or shortly thereafter by the ingestion of infected colostrum and/or milk. Lateral transmission via a respiratory route has also been documented in older sheep. The importance of each route may vary between flocks and management practices. Even in flocks that have a significant rate of infection, the manifestation of clinical disease is low. Clinical disease is not apparent before 2 years of age and is most common after 3 years. The disease develops insidiously with
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition the earliest sign being a loss of body condition, which is why this disease is sometimes called “thin ewe syndrome.” Dyspnea develops later and may lead to exercise intolerance, causing a ewe to fall behind the rest of the flock. In some cases there is mammary gland or joint involvement. The disease is also known as “hard bag.” The milk is normal in appearance but there is little to no volume. Economic losses associated with OPP are primarily the result of premature culling, the loss of value for the mature clinically affected animals, mortalities, and the possible effects of subclinical infection on productivity. A review of other countries’ import regulations indicates that these may be barriers to U.S. sheep. Once OPP has been introduced into a flock it is difficult and costly to eradicate because there is no treatment. If a flock is free of OPP, considerable effort should be made to maintain this status and prevent introduction of the disease. Control may be attempted by segregating lambs at birth and hand raising them on bovine milk or milk replacers. Another strategy is to test and cull serologically positive animals and their offspring (Radostits et al., 2007). Seroprevalence of OPP was measured during the 2001 NAHMS sheep study by testing sheep on randomly selected sheep operations. More than 21,000 samples collected at 682 operations were tested. The seroprevalence was calculated to be 24.2 percent. Overall, 36.4 percent of the operations had one or more positive animals (USDA, 2003c). Contagious Ecthyma Contagious ecthyma, also called soremouth or orf, is caused by the orf virus, genus Parapoxvirus. It is commonly introduced into a flock by the purchase of new animals or by contact with other sheep at fairs and shows. Soremouth most commonly affects young lambs but may also affect adult sheep, especially in previously unexposed flocks. The animals develop papules on the lips and mouth with occasional involvement of the udder and teats. The papules progress to vesicles and then scabs. The virus remains infectious in the scabs for long periods under dry conditions. Once infected, the immunity in a sheep lasts for many years; however, this immunity is not transferred via colostrum, and hence newborn lambs are susceptible. In flocks with preexisting immunity the economic impacts are usually minor. More severe financial losses may occur if very young animals develop lesions severe enough to interfere with nursing. This would also be true if lesions develop on the teats of lactating ewes. The disease can be zoonotic, but most people recover uneventfully (Radostits et al., 2007).
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition Caseous Lymphadenitis (CL) Caseous lymphadenitis (CL) can be of considerable economic importance to the sheep industry because it results in reduced growth weights, reduced fleece weights, and carcass condemnation. The disease affects both sheep and goats and is a chronic recurring disease. Sheep are usually exposed to the organism through skin or mucous membranes, but the bacteria usually enter through wounds or abrasions. The source of the bacterial agent (Corynebacterium pseudotuberculosis) can be abscesses on the sheep, the environment, or equipment (especially shearing equipment). The pus contains large amounts of bacteria that can survive in bedding and soil for many months. Sheep infected with CL present with abscesses especially around the head and neck, and the number of abscesses usually increases with age. Most often, the abscesses are in surface lymph nodes but can become systemic and appear in internal nodes and organs (e.g., lungs and liver). An initial infection may result in no clinical signs; however, as the animal ages, this changes. The disease may contribute to “thin animal syndrome.” Bronchopneumonia, abortion, arthritis, and central nervous system abscesses may occur with CL infection, but these are not common findings. A diagnosis of CL is usually made using history and clinical signs. The organism may be cultured. Although there are serological tests available, they have limitations because infected animals may test negative if abscesses are walled off, young animals (< 6 months) may test positive because of colostrum titers, and vaccinated animals will test positive. Treating animals infected with CL with antibiotics is not effective. Animals with signs should be culled. Because shearing is one of the primary means of within-flock transmission, older animals should be shorn last. The vaccine reduces incidence and prevalence, but it will not cure the disease and will not prevent new infections. Because eradication is extremely difficult, prevention is key (Radostits et al., 2007). Johne’s Disease Johne’s disease, which is caused by Mycobacterium avium paratuburculosis, causes a wasting condition in sheep for which there is no vaccine in the United States and no treatment. Like OPP, elimination of Johne’s disease from a flock is difficult and expensive. Johne’s disease also has trade implications for sheep exported from the United States. The disease is discussed in greater detail in sections below.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition Ram Epididymitis (RE) Ram epididymitis is more common in western range flocks and commonly introduced with the purchase or use of infected rams. The organism responsible for RE is Brucella ovis. Rams infected with B. ovis have reduced fertility or may be sterile. The disease may influence the number of rams required. Lambing percentages may be reduced by 30 percent in recently infected flocks and by 15–20 percent in flocks with endemic infection. In flocks that have a prevention/control program for RE, there is an additional return of $12.00 per ewe mated (Kimberling and Schweitzer, 1989). Ewes are somewhat resistant, but the disease may cause early embryonic death and, in some cases, abortion (Radostits et al., 2007). Scrapie Scrapie is an insidious, degenerative disease affecting the central nervous system of sheep, goats, and moufflon. Scrapie is discussed in detail later in this chapter. Internal Parasites (Resistant Worms) Internal parasites are addressed in the section on diseases of economic impact or concern. Recordkeeping To maximize profitability, it is imperative that production parameters including disease status are measured. Accurate assessments of production efficiency cannot be made without records and identification. Without records, there are no yardsticks by which to measure possible problems and improvements. Records provide a baseline and can assist in determining which management practices help improve the operation and which may add costs without return. Without records, many of the silent inefficiency losses caused by disease may go unnoticed. The NAHMS 1996 Sheep Health and Management Practice study found that almost 20 percent of producers kept no records (USDA, 1996). In 2001, the study found that slightly over 30 percent did not keep records (USDA, 2002). The study did not go into detail about which specific records were kept or what production parameters were recorded. Records that would assist in evaluating the overall health status of a flock include the number of ewes exposed to the ram, any abortions and cause, number of lambs born, number of live lambs born, reason for lamb deaths, birth weights, body and udder condition of the ewe, condition of the colostrum, any apparent clinical disease conditions,
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition any serological or other evidence of disease, necropsy results, number of lambs at weaning, weaning weights, yearling weights, vaccinations given, treatments, cost of the treatment (including labor), and number of animals culled and reason for culling. Identification Another important component of flock management and disease control is identification. Identification is critical for timely tracing of disease spread and eventual elimination. In addition, if animals are not identified, measuring production efficiency is difficult especially in relationship to the cost of disease. The 2001 NAHMS study found that 27.4 percent of all operations participating in the survey used flock identification (all animals have the same identification), of which more than 87 percent of the operations with flocks over 1,000 head used flock identification (USDA, 2002). Perhaps most important, the 2001 NAHMS study found that 80 percent of all operations used some form of individual identification, including 68 percent of the large flocks (> 1,000 head), emphasizing the importance of identification if scrapie is ever to be eliminated from the United States. Hence, in November 2001, a federal regulation requiring the identification of certain classes of sheep went into effect (Federal Register, 2001). The statistics mentioned above reflected industry practices prior to this regulation. The sheep industry has a more complete ID system than exists for any other species in the United States at this time. Three national sheep industry programs have an identification component, including the National Scrapie Eradication Program (NSEP), the Scrapie Flock Certification Program (SFCP), and the National Animal Identification Program (NAIS). Only the NSEP is mandatory. National Scrapie Eradication Program (NSEP) Regulations Near the end of 2001, final regulations for the NSEP were published under Title 9, Part 79 of the Code of Federal Regulations (CFR; Federal Register, 2001). These regulations require official identification for sheep and goats moving interstate. The purposes of the regulations were to provide a more effective national program for scrapie surveillance and to facilitate the traceback of scrapie-positive animals. The lack of identification and records was found to be hampering scrapie control efforts Animals required to be identified in 9 § CFR 79.3 must be officially identified to the flock of birth upon change of ownership. In cases where the flock of birth cannot be determined, the animal is to be officially identi-
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition fied to the flock of origin (flock in which an animal most recently resided for breeding). Animals required to be officially identified include: All breeding sheep; All sexually intact animals for exhibition; All sheep over 18 months of age; All exposed and high-risk animals including all low-risk exposed animals, genetically susceptible exposed animals, genetically less susceptible exposed animals, and genetically resistant exposed sheep; All suspect and test-positive animals; Animals from noncompliant flocks; Breeding goats, except low-risk commercial goats. Animals not required to be individually identified include: Slaughter sheep (sheep in slaughter channels) under 18 months. (Note: If a sexually intact sheep is sold at an unrestricted sale [any sale that is not a slaughter or feeding for slaughter sale], it must be identified. If these animals cannot be identified to flock of origin, they must be identified with slaughter only tags); Wethers for exhibition and wethers under 18 months of age; Slaughter goats (goats in slaughter channels); Low-risk commercial goats; Animals shipped directly to an approved slaughter facility or an approved market when all the animals in a section of a truck are from the same premises of origin and are accompanied by an owner’s statement. (Note: The owner’s statement must contain the information needed for the plant or market to identify the animals); Animals moved for grazing or similar management reasons whenever the animals are moved from a premises owned or leased by the owner of the animals to another premises owned or leased by the owner of the animals. Under NSEP rules, the flock is assigned a premise number and the identification and movement information must be recorded. These records must be retained for at least 5 years after the date of the movement. Lambs under 18 months of age moving to slaughter and animals not leaving the premise do not have to be identified. Some states have additional restrictions for sheep moving within the state for shows, sales, and other events. The identification requirements are a part of the scrapie eradication effort. In the event that scrapie is eliminated from the United States and/or there is no longer a program, the identification requirements may not be applicable, potentially hampering other management practices. To some
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition extent, this is what happened in the cattle industry where identification was linked to the brucellosis program. As brucellosis was eliminated, identification and records were no longer available for managing other diseases. Scrapie Flock Certification Program (SFCP) The SFCP monitors flocks over time and confers a certified status on those that do not have evidence of the disease after a minimum of 5 years complying with movement, identification, recordkeeping, and sampling requirements. The basis of this program is to provide a source of sheep having a negligible risk of scrapie for domestic and international markets. The SFCP requires that the following sheep within a flock enrolled in the complete or export-monitored category be identified with a program-approved ID such as an official eartag: All animals one year of age or older; All acquired animals before commingling with the flock unless already identified with an approved device; and All sexually intact animals < 1 year old with a change of ownership unless moving directly to slaughter or to a terminal feedlot. National Animal Identification System (NAIS) After the first case of bovine spongiform encephalopathy (BSE) was detected in the United States in 2003, there was a movement to develop and implement a nationwide identification and tracing (recordkeeping) system (now known as the National Animal Identification System or NAIS), which could trace animal movements in 48 hours. After the initial public and media reaction subsided, certain livestock species groups began to withdraw support for a mandatory identification program and urged the U.S. Department of Agriculture (USDA) to implement a voluntary national identification program. Other species groups still support the need for a mandatory system. Currently, USDA has taken the position that every aspect of the NAIS will be voluntary in nature. The NAIS is an identification and information system consisting of three components, all of which are voluntary: (1) premises registration, (2) animal identification, and (3) tracing. An owner may choose only to register a premise and not participate with animal identification or tracing. The premises registration component of the NAIS ensures the availability of a nationwide communications network to assist livestock owners and animal health officials in the event of an animal disease emergency. Upon registering with a state or tribal animal health authority, a premise is assigned a unique
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition have not raised livestock before. The lack of practitioners to give advice, administer treatments, perform surgeries, and euthanize animals may lead to prolonged and unnecessary suffering. Lack of death loss data. An accurate estimate of the actual lamb crop in the United States cannot be developed without death loss data for the predocking period in some of the states with the highest sheep numbers. More important, efforts to reduce such losses are encumbered without an accurate baseline that could provide answers to various questions, such as the following relating to possible reasons for lower numbers of lambs: Are the ewes giving birth to multiple lambs? Are lambs born dead? Are lambs dying shortly after birth from no colostrum or poor mothering? Are lambs dying at a few weeks of age from scours, pneumonia, and other causes? Are predators responsible for the majority of deaths? Monitoring research on atypical scrapie. With the tremendous progress the industry and USDA have made in reducing the prevalence of classical scrapie, it will be important for all parties to continue to monitor the changing science and epidemiology surrounding atypical scrapie, especially the theories on origin, routes of transmission, and the effects of genetics. What is almost certain is that the current genetic approach as used around the world will not work for atypical scrapie. It may be that other genotypes could be considered but even that is unknown. Research on the link between MAP and Crohn’s disease. If a scientific consensus is reached or if a definitive link is found between MAP and Crohn’s, the sheep industry may find itself in a precarious position on a food safety issue. In a crisis, the unknowns are considered one of the biggest enemies. Currently the industry does not know the prevalence of OJD, if cooking kills the agent, or if pasteurization of sheep’s milk is more effective than pasteurization of cow’s milk. It is important to begin research in these areas. REFERENCES Agra CEAS Consulting. 2007. The World Organization for Animal Health (OIE) Prevention and control of animal diseases worldwide economic analysis, prevention versus outbreak costs. Final Report, Part I. Online at: http://www.oie.int/eng/OIE-WB_Conference_1007/OIE%20Economic%20Studies/OIE%20-%20Cost-Benefit%20Analysis%20(Part%20I).pdf. Accessed April 6, 2008.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition Andréoletti, O., S. Simon, C. Lacroux, N. Morel, G. Tabouret, A. Chabert, S. Lugan, F. Corbiere, P. Ferre, G. Foucras, H. Laude, F. Eychenne, J. Grassi, and F. Schelcher. 2004. PrPSc accumulation in myocytes from sheep incubating natural scrapie. Nat. Med. 10:591–593. Barger, I. A., and K. M. Dash. 1987. Repeatability of ovine faecal egg counts and blood packed cell volumes in Haemonchus contortus infections. Int. J. Parasitol. 17:977–980. Benestad, S. L., P. Sarradin, B. Thu, J. Schönheit, M. A. Tranulis, and B. Bratberg. 2003. Cases of scrapie with unusual features in Norway and designation of a new type Nor98. Vet. Rec. 153:202–208. Brown, J. P., and J. D. Silverman. 1999. The current and future market for veterinarians and veterinary medical services in the United States. J. Am. Vet. Med. Assoc. 215:161–183. Brown, P., F. Cathala, R. F. Raubertas, D. C. Gajdusek, and P. Castaigne. 1987. The epidemiology of Creutzfeldt-Jakob disease: Conclusion of a 15-year investigation in France and review of the world literature. Neurology 37:895–904. Brown, P., and D. C. Gajdusek. 1991. Survival of scrapie virus after 3 years’ interment. Lancet 337:269–270. Buschmann, A., A.-G Biacabe, U. Ziegler, A. Bencsik, J.-Y Madec, G. Erhardt, G. Lühken, T. Baron, and M. H. Groschup. 2004. Atypical scrapie cases in Germany and France are identified by discrepant reaction patterns in BSE rapid tests. J. Virol. Methods 117:27–36. Casalone, C., C. Corona, M. I. Crescio, F. Martucci, M. Mazza, G. Ru, E. Bozzetta, P. L. Acutis, and M. Caramelli. 2005. Pathological prion protein in the tongues of sheep infected with naturally occurring scrapie. J. Virol. 79:5847–5849. Craig, T. M. 2006. Anthelmintic resistance and alternative control methods. Vet. Clin. N. Am. Food Anim. Pract. 22:567–581. De Brosschere, H., S. Roels, S. J. Benestad, and E. Vanopdenbosch. 2004. Scrapie case similar to Nor98 diagnosed in Belgium via active surveillance. Vet. Rec. 155:707–708. Detwiler, L. A., and M. Baylis. 2003. The epidemiology of scrapie. Rev. Sci. Tech. Office International des Epizooties (OIE) 22(1):121–143. Detwiler, L. A., A. L. Jenny, R. Rubenstein, and N. E. Wineland. 1997. Scrapie: a review. Sheep Goat Res. J. 12(3):111–131. Dickinson, A. G., J. T. Stamp, and C. C. Renwick. 1974. Maternal and lateral transmission of scrapie in sheep. J. Comp. Pathol. 84:19–25. Eloit, M., K. Adjou, M. Coulpier, J. J. Fontaine, R. Hamel, T. Lilin, S. Messiaen, O. Andréoletti, T. Baron, A. Bencsik, A. G. Bicae, V. Beringue, H. Laude, G. LeDu, J. L. Vilotte, E. Comoy, S. P. Deslys, J. Grassi, S. Simon, F. Lantier, and P. Sarradin. 2005. BSE agent signature in a goat . Vet. Rec. 156:523–524. Epstein, V., S. Panting, and S. Halfacre. 2005. Atypical scrapie in the Falkland Islands. Vet. Rec. 157:667–668. European Community. 2007. A new animal health strategy for the European Union (2007–2013) where “Prevention is better than cure.” Online at: http://ec.europa.eu/food/animal/diseases/strategy/animal_health_strategy_en.pdf. Accessed April 29, 2008. European Union. 2006. Report on Monitoring and Testing of Ruminants for Transmissible Spongiform Encephalopathy (TSE) in the EU in 2006. Online at: http://ec.europa.eu/food/food/biosafety/bse/annual_report_tse2006_en.pdf. Accessed November 28, 2007. Federal Register. 2001, August 21. Rules and Regulations, 9 CFR Parts 54 and 79.66(162): 43963–44003. Gavier-Widen, D., M. Noremark, S. Benestad, M. Simmons, L. Renstrom, B. Bratberg, M. Elvander, and C. H. Segerstad. 2004. Recognition of Nor98 variant of scrapie in the Swedish sheep population. J. Vet. Diagn. Invest. 16:562–567.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition González, L., M. Jeffrey, S. Sisó, S.Martin, S. J. Bellworthy, M. Stack, M. Chaplin, L. Davis, M. Dagleish, and H. Reid. 2005. Diagnosis of preclinical scrapie in samples of rectal mucosa. Vet. Rec. 156:846–847. Grant, I. R., H. J. Ball, and M. T. Rowe. 2002. Incidence of Mycobacterium paratuberculosis in bulk raw and commercially pasteurized cows’ milk from approved dairy processing establishments in the United Kingdom. Appl. Environ. Microbiol. 68:2428–2435. Groschup, M. H., F. Weiland, O. C. Straub, and E. Pfaff. 1996. Detection of scrapie agent in the peripheral nervous system of a diseased sheep. Neurobiol. Dis. 3:191–195. Groschup, M. H., C. Lacroux, A. Buschmann, G. Lühken, J. Mathey, M. Eiden, S. Lugan, C. Hoffman, J. C. Espinosa, T. Barron, J. M. Torres, G. Erhardt, and O. Andréoletti. 2007. Classic scrapie in sheep with the ARR/ARR prion genotype in Germany and France. Emerg. Infect. Dis. 13:1201–1207. Hadlow, W. J., R. E. Race, R. C. Kennedy, and C. M. Eklund. 1979. Natural infection of sheep with scrapie virus. Pp. 3–12 in Slow Transmissible Diseases of the Nervous System,Vol. 2, S. B. Prusiner and W. J. Hadlow, eds. New York: Academic Press. Hadlow, W. J., R. C. Kennedy, and R. E. Race. 1982. Natural infection of Suffolk sheep with scrapie virus. J. Infect. Dis. 146:657–664. Harries Jones, R., R. Knight, R. G. Will, S. N. Cousens, P. G. Smith, and W. B. Mathews. 1988. Creutzfeldt-Jakob disease in England and Wales, 1980–1984: A case-control study of potential risk factors. J. Neurol. Neurosurg. Psych. 51:1113–1119. Hoinville, L. J., A. Hoek, M. B. Gravenor, and A. R. McLean. 2000. Descriptive epidemiology of scrapie in Great Britain: Results of a postal survey. Vet. Rec. 146:455–461. Hopp, P., M. K. Omer, and B. T. Heier. 2006. A case-control study of scrapie Nor98 in Norwegian sheep flocks. J. Gen. Virol. 87:3729–3736. Hunter, N. 1997. Molecular biology and genetics of scrapie in sheep. Pp. 225–240 in The Genetics of Sheep, L. Piper and A. Ruvinsky, eds. Wallingford, UK: CABI Publishing. Hunter, N., W. Goldmann, G. Smith, and J. Hope. 1994. The association of a codon 136 PrP gene variant with the occurrence of natural scrapie. Arch. Virol. 137:171–177. Hunter, N., J. D. Foster, W. Goldmann, M. J. Stear, J. Hope, and C. Bostock. 1996. Natural scrapie in a closed flock of Cheviot sheep occurs only in specific PrP genotypes. Arch. Virol. 141:809–824. Hunter, N., D. Cairns, J. D. Foster, G. Smith, W. Goldmann, and K. Donnelly. 1997. Is scrapie solely a genetic disease? Evidence from scrapie-free countries. Nature 386:137. Hunter, N., J. D. Foster, A. Chong, S. McCutcheon, D. Parnham, S. Eaton, C. MacKenzie, and F. Houston. 2002. Transmission of prion diseases by blood transfusion. J. Gen. Virol. 83:2897–2905. Kaplan, R. M. 2004. Drug resistance in nematodes of veterinary importance: a status report. Trends Parasitol. 20:477–481. Kimberling, C. V., and D. Schweitzer. 1989. Brucella ovis infection and its management in ovine reproduction. Agri-Practice 10:36–39. Konold, T. 2008. Evidence of scrapie transmission via milk. BMC Vet. Res. 4:14. Le Dur, A., V. Béringue, O. Andréoletti, F. Reine, T. L. Laï, T. Baron, B. Bratberg, J. L. Viloe, P. Saradin, S. L. Benestad, and H. Laude. 2005. A newly identified type of scrapie agent can naturally infect sheep with resistant PrP genotypes. Proc. Nat. Acad. Sci. U. S. A. 102:16031–16036. Ligios, C., C. J. Sigurdson, C. Santucciu, G. Carcassola, G. Manco, M. Basagni, C. Maestrale, M. G. Cancedda, L. Madau, and A. Aguzzi. 2005. PrPsc in mammary glands of sheep affected by scrapie and mastitis. Nat. Med. 11:1137–1138. Lühken, G., A. Buschmann, H. Brandt, M. Eiden, M. Groschup, and G. Erhardt. 2007. Epidemiological and genetical differences between classical and atypical scrapie cases. Vet. Res. 38:65–80.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition Millar, D., J. Ford, J. Sanderson, S. Withey, M. Tizard, T. Doran, and J. Hermon-Taylor. 1996. IS900 PCR to detect Mycobacterium paratuberculosis in retail supplies of whole pasteurized cows’ milk in England and Wales. Appl. Environ. Microbiol. 62:3446–3452. Moum, T., I. Olsaker, P. Hopp, T. Moldal, M. Valheim, and S. L. Benestad. 2005. Polymorphisms at codons 141 and 154 in the ovine prion protein gene are associated with scrapie Nor98 cases. J. Gen. Virol. 86:231–2235 NAIS (National Animal Identification System). 2006. Sheep Working Group Report, August. Online at: http://www.sheepusa.org/?page=site/text&nav_id=bbe4ac2bced3271a5a89002b58b479de. Accessed November 27, 2007. NIAA (National Institute for Animal Agriculture). 2003. The ABCs of genetic based flock clean-up and monitoring plans. National Scrapie Education Initiative. Bowling Green, KY. OIE (World Organization for Animal Health). 2007. Terrestrial animal health code, Chapter 2. Paris, France. Online at: http://www.oie.int/eng/normes/mcode/en_partie_2.htm and at: http://www.oie.int/eng/normes/mcode/en_chapitre_2. 3.13.htm. Accessed April 29, 2008. Onodera, T., T. Ikeda, Y. Muramatsu, and M. Shinagawa. 1993. Isolation of scrapie agent from the placenta of sheep with natural scrapie in Japan. Microbiol. Immunol. 37:311–316. O’Rourke, K. I., T. V. Baszler, T. E. Besser, J. M. Miller, R. C. Cutlip, G. A. H. Wells, S. J. Ryder, S. M. Parish, A. N. Hamir, N. E. Cockett, A. Jenny, and D. P. Knowles. 2000. Preclinical diagnosis of scrapie by immunohistochemistry of third eyelid lymphoid tissue. J. Clin. Microbiol. 38:3254–3259. Parry, H. B. 1983. Pp. 31–51 in Scrapie Disease in Sheep, D. R. Oppenheimer, ed. New York: Academic Press. Pattison, I. H., and G. C. Millson. 1962. Distribution of the scrapie agent in the tissue of experimentally inoculated goats. J. Comp. Pathol. 72:233–244. Pattison, I. H., M. N. Hoare, J. N. Jebbett, and W. A. Watson. 1972. Spread of scrapie to sheep and goats by oral dosing with foetal membranes from scrapie-affected sheep. Vet. Rec. 90:465–468. Pattison, I. H., M. N. Hoare, J. N. Jebbett, and W. A. Watson. 1974. Further observations on the production of scrapie in sheep by oral dosing with foetal membranes from scrapie affected sheep. Br. Vet. J. 130 (4):lxv–lxvii. Prince, J. B., D. M. Andrus, and K. P. Gwinner. 2006. Future demand, probable shortages, and strategies for creating a better future in food supply veterinary medicine. J. Am. Vet. Med. Assoc. 229(1):57–69. Race, R., A. Jenny, and D. Sutton. 1998. Scrapie infectivity and proteinase K-resistant prion protein in sheep placenta, brain, spleen, and lymph node: Implications for transmission and antemortem diagnosis. J. Infect. Dis. 178:949–953. Radostits, O. M., C. C. Gay, K. W. Hinchcliff, and P. D. Constable (eds). 2007. A Textbook of the Diseases of Cattle, Horses, Sheep, Pigs and Goats, 10th edition, New York: Saunders Elsevier. Ralph, A., M. V. N. O’Sullivan, N. C. Sangster, and J. C. Walker. 2006. Abdominal pain and eosinophilia in suburban goat keepers. Med. J. Aust. 184:467–469. Schreuder, B. E. C., M. C. M. de Jong, J. J. Pekelder, P. Vellema, A. J. M. Broker, and H. Betcke. 1993. Prevalence and incidence of scrapie in the Netherlands: A questionnaire survey. Vet. Rec. 133:211–214. SEAC (Spongiform Encephalopathy Advisory Committee). 2007. Minutes of the 96th meeting held on February 20, 2007, London, England. Online at: http://www.seac.gov.uk/minutes/final96.pdf. Accessed April 29, 2008. Seaman, J., and M. Evers. 2006. Foot rot in sheep and goats. Fact Sheet New South Wales Department of Primary Industries. Online at: http://www.dpi.nsw.gov.au/__data/assets/pdf_file/0015/102381/footrot-in-sheep-and-goats.pdf. Accessed April 6, 2008.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition Seidel, B., A. Thomzig, A. Buschmann, M. H. Groschup, R. Peters, M. Beekes, and K. Terytze. 2007. Scrapie agent (Strain 263K) can transmit disease via the oral route after persistence in soil over years. PLoS ONE 2(5):e435. Seitzinger, A. H., P. L. Paarlberg, and J. G. Lee. 2006. Economic impacts of eradicating scrapie, ovine progressive pneumonia, and Johne’s Disease on U.S. sheep, lamb, sheep meat, and lamb meat markets. Pp. 193–206 in The Economics of Livestock Disease Insurance, S. R. Koontz D. L. Hoag, D. D. Thilmany, J. W. Green, and J. L. Grannis, eds. Wallingford, UK: CABI Publishing. Sigurdarson, S. 1991. Epidemiology of scrapie in Iceland and experience with control measures. Pp. 233–242 in Sub-acute Spongiform Encephalopathies, R. Bradley, M. Savey, and B. Marchant, eds. Boston: Kluwer Academic Publishers. Thompson, D., P. Muriel, D. Russell, P. Osborne, A. Bromley, M. Rowland, S. Creigh-Tyte, and C. Brown. 2002. Economic costs of the foot and mouth disease outbreak in the United Kingdom in 2001. Rev. Sci. Tech. Office International des Epizooties (OIE) 21:675–687. USDA (U.S. Department of Agriculture). 1996. Reference of 1996 sheep health and management practices. National Animal Health Monitoring System. Animal and Plant Health Inspection Service. Fort Collins, CO, September. USDA. 2000. Declaration of emergency because of scrapie in the United States. Federal Register, Vol. 65, No. 53, p. 14521, March 17. USDA. 2002. Part 1: Reference of sheep management in the United States, 2001. USDA: APHIS:VS, CEAH, National Animal Health Monitoring System, Fort Collins, CO, No. N3560702. USDA. 2003a. Part II: Reference of sheep management in the United States, 2001. USDA: APHIS:VS, CEAH, National Animal Health Monitoring System, Fort Collins, CO, No.N3780403. USDA. 2003b. Part III: Lambing Practices, Spring 2001. APHIS:VS, CEAH, National Animal Health Monitoring System, Fort Collins, CO, No. N3790403. USDA. 2003c. Fact Sheet on Ovine Progressive Pneumonia. Online at: http://www.aphis.usda.gov/vs/ceah/ncahs/nahms/sheep/sheep01/OPP.pdf. Accessed November 28, 2007. USDA. 2003d. Phase II: Scrapie: Ovine Slaughter Surveillance Study, 2002–2003. APHIS: VS,CEAH, National Animal Health Monitoring System, Fort Collins, CO, No. N419.0104. USDA. 2003e. Scrapie Ovine Slaughter Surveillance Info Sheet. Online at: http://www.aphis.usda.gov/vs/ceah/ncahs/nahms/sheep/SOSSphase1.pdf. Accessed November 28, 2007. USDA. 2004. Ovine Johnes Disease: Awareness, Management and Seroprevalence. National Animal Health Monitoring System, Animal and Plant Health Inspection Service, Fort Collins, CO. USDA. 2005. Sheep and lamb nonpredator death loss in the United States, 1999. National Animal Health Monitoring System, Animal and Plant Health Inspection Service, Fort Collins, CO, December. USDA. 2006. 2004–2006 Subcommittee: Assessment of the Food Safety Importance of Mycobacterium avium subspecies paratuberculosis (MAP). National Advisory Committee on Microbiological Criteria for Foods, Food Safety and Inspection Service, Washington, DC. Online at: http://www.fsis.usda.gov/About_ FSIS/NACMCF_Subcommittee_MAP/index.asp. Accessed April 29, 2008. USDA. 2007a. Scrapie Program Report, FY 2006, Veterinary Services, Animal and Plant Health Inspection Service, February 5. Online at: http://www.aphis.usda.gov/animal_health/animal_diseases/scrapie/downloads/yearly_report_2006.pps. Accessed September 20, 2007.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition USDA. 2007b. Scrapie Program September Monthly Report, FY 2007, Veterinary Services, Animal and Plant Health Inspection Service, February 5. Online at: http://www.aphis.usda.gov/animal_health/animal_diseases/scrapie/downloads/monthly_scrapie_rpt.pps#264,1,Scrapie Program. Accessed November 28, 2007. U.S. HHS (U.S. Department of Health and Human Services). 1997. Substances prohibited from use in animal food or feed: Animal proteins prohibited in ruminant feed. Regulatory impact analysis. U.S. HHS, FDA, and AEI-Brookings Joint Center for Regulatory Studies. RIN: 0910-AA91, Federal Register 62(June 5):30396. van Keulen, L. J., B. E. Schreuder, R. H. Meloen, G. Mooij-Harkes, M. E. Vromans, and J. P. Langeveld. 1996. Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. J. Clin. Microbiol. 34:1228–1231. van Keulen, L. J., B. E. Schreuder, M. E. Vromans, J. P. Langeveld, and M. A. Smits. 1999. Scrapie-associated prion protein in the gastrointestinal tract of sheep with natural scrapie. J. Comp. Pathol. 121:55–63. Westaway, D., V. Zuliani, C. Cooper, M. D. Costa, S. Neuman, A. L. Jenny, L. A. Detwiler, and S. B. Prusiner. 1994. Homozygosity for prion protein alleles encoding glutamine-171 renders sheep susceptible to natural scrapie. Genes Dev. 8:959–969. WHO (World Health Organization). 1999. WHO consultation on public health and animal transmissible spongiform encephalopathies: Epidemiology, risk and research requirements, with the participation of the Office International des Epizooties, 1–3. Geneva, December. Online at: www.who.int/csr/resources/publications/bse/WHO_CDS_CSR_APH_2000_2/en/pdf. Accessed March 12, 2007. Woolhouse, M. E. J., and S. Gowtage-Sequeria. 2005. Host range and emerging and reemerging pathogens. Emerg. Infect. Dis. 11:1842–1847. Wyoming Livestock Board. 2007. NOR98-like strain of scrapie found in Wyoming. Press Release, March 17, 2007. Cheyenne, WY. Online at: http://wlsb.state.wy.us/NewReleases/07Mar16FINALNOR98LIKESCRAPIEPRESSRLS.pdf. Accessed April 29, 2008. Young, G. B., J. T. Stamp, C. C. Renwick, and A. G. Dickinson. 1964. Field observations on scrapie incidence. Pp. 199–206 in Report of Scrapie Seminar (ARS 91–53), January 27–30, 1964. Washington, DC: ARS. Zajac, A. M. 2006. Gastro-intestinal nematodes of small ruminants: life cycle, anthelmintics, and diagnosis. Vet. Clin. N. Am. Food Anim. Pract. 22:529–541.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition APPENDIX: A CHRONOLOGY OF SCRAPIE CONTROL IN THE UNITED STATES 1947 – First case of scrapie was diagnosed in a Michigan flock. The sheep were of British origin imported from Canada over a period of years. 1952 – Scrapie diagnosed in a California flock. Insistence from the United States Animal Health Association (USAHA) prompted the U. S. Secretary of Agriculture to declare a state of emergency to handle the disease. The eradication program included laboratory confirmation, quarantine and depopulation of infected flocks, and tracing and slaughter of exposed animals sold from infected flocks. The federal indemnity paid at this time was 50 percent of the difference between the appraised value of the animal and salvage, but not to exceed $25.00 per head for grade animals and $75.00 for purebreds. 1953 – The Act of 1884 was amended to include scrapie, and the emergency order was rescinded. 1954 – Title 9 Code of Federal Regulations Part 54 was promulgated. These regulations covered animals destroyed because of scrapie. 1955 – Regulations were amended to include goats. 1957 – Program was broadened to include source flocks. These were defined as flocks from which an affected animal was removed within 18 months before showing signs of scrapie. The source flock was also quarantined and depopulated. Exposed animals sold from the source flocks were traced and slaughtered. 1964 – Scrapie Field Trials began at Mission, Texas. 1965 – The widespread eradication program was modified to allow a provision for bloodline slaughter. In the event the disease was limited to one bloodline, slaughter could be confined to that genetic line. The nonbloodline animals were placed under 2 year quarantine with sale to slaughter only. After the quarantine period, the animals were subject to 18 months of surveillance. In lieu of the bloodline option the owner could opt to depopulate the entire flock. Note: Although the bloodline program was in effect for 10 years, the bloodline option was used in only 4 of some 71 cases.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition 1975 – Bloodline option was eliminated. Exposed animals could no longer be slaughtered for human consumption due to a perceived public health risk. Federal indemnity was increased to $40 for grades and $90 for purebreds. 1978 – Federal indemnity was paid in the amount of two-thirds of the appraised value of the animal not to exceed $300. This formula was used for both grades and purebreds. 1980 – Canada adopts a bloodline program. 1982 – On recommendations by USAHA and the National Woolgrowers Association, the Cooperative Scrapie Eradication Program was reviewed. 1983 – The Scrapie Eradication Program as outlined in Veterinary Services Memorandum 557.1, dated April 8, 1983, went into effect. The program involved diagnosing infected animals, tracing and euthanizing bloodline animals, and maintaining infected and bloodline flocks under surveillance. The program concentrated primarily on the elimination of bloodline animals on the maternal side. The rationale for this change was to reduce indemnity payments and preserve valuable bloodlines without supposedly reducing the effectiveness of the program. 1987–1988 – Scrapie Review meetings held. These reviews involved representatives from industry, researchers, state regulators, and USDA APHIS. Advanced notice in the Federal Register of proposed rulemaking, soliciting comments on whether to discontinue the Scrapie Eradication Program. Comments received in response to this rulemaking overwhelmingly asked APHIS not to discontinue efforts to control scrapie. The commentators did request that the government officials in cooperation with industry groups devise a new program for the control of scrapie. 1990 – Scrapie Negotiated Rulemaking Committee established.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition The following organizations were represented on the Rulemaking Committee: American Association of Small Ruminant Practitioners American Farm Bureau American Hampshire Association American Meat Institute American Polypay Association American Sheep Industry, Inc. American Suffolk Society Animal and Plant Health Inspection Service Continental Dorset Club National Assembly of Chief Livestock Health Officials National Renderers Association National Suffolk Association United States Animal Health Association 1991 – The Rulemaking Committee agreed upon a core program for the control of scrapie. This program consists of the following facets: A voluntary scrapie flock certification program; One-time indemnification for infected and source flocks; and Regulations to establish identification of sheep from scrapie-infected and source flocks moving in interstate. 1992 – Voluntary Scrapie Flock Certification Program (VSFCP) established. Interstate regulations to identify sheep from scrapie-infected and source flocks established (Detwiler et al., 1997). 1997 – VSFCP modified to make it more user friendly for commercial producers. 1999 – APHIS reviewed and revised the VSFCP which became the Scrapie Flock Certification Program. 2001 – APHIS approves the third eyelid test for the diagnosis of scrapie in live sheep. APHIS makes official eartags available to producers, dealers, and markets.
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Changes in the Sheep Industry in the United States: Making the Transition from Tradition Federal regulations that enacted the NSEP went into effect: (1) Records and identification required for sheep moving in interstate commerce, (2) indemnity was reinstated and (3) a program to recognize states that conducted an active scrapie control program consistent with federal requirements was established. Phase 1 of the Scrapie Slaughter Surveillance Study (SOSS) began. 2002 – Phase 2 of the Scrapie Slaughter Surveillance Study began. This phase was carried out to determine the prevalence of scrapie in the United States. 12,491 valid test results were obtained. It was determined that the overall weighted national prevalence of scrapie in mature sheep was 0.20 percent. More details are provided below. APHIS adopted a genetics-based flock clean-up plan as a standard method for cleaning up scrapie-infected flocks. 2003 – USDA received $15 million in appropriated funding to conduct NSEP. SOSS concluded and the Regulatory Scrapie Slaughter Surveillance began. Scrapie Eradication Uniform Method and Rules published. APHIS approved the immunohistochemistry on lymphoid tissue as an official test. National Identification Development Team (NIDT) Steering Committee created. 2004 – SOSS results published. Sheep-specific animal identification plan was presented to the NIDT Steering Committee. 2007 – APHIS received $18.4 million in appropriated funds to conduct NSEP. 2010 – Goal to eliminate scrapie outbreaks in the United States. 2017 – Goal for the United States to be declared “scrapie-free” by the World Organization for Animal Health (OIE) (D. Sutton, personal communication, 2007).
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