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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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Suggested Citation:"3 Sheep Health Issues." National Research Council. 2008. Changes in the Sheep Industry in the United States: Making the Transition from Tradition. Washington, DC: The National Academies Press. doi: 10.17226/12245.
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3 Sheep Health Issues M aintaining the health of a flock is imperative for a successful sheep operation because disease imposes both apparent as well as hid- den 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 deter- mination 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; 121

122 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES • 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 impli- cations 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 cri- sis resulting from a highly contagious or zoonotic disease outbreak. To pre- vent 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 preven- tion 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;

SHEEP HEALTH ISSUES 123 • 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 (treat- ment 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 pro- vides useful advice. 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 dis- ease 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, treat- ments 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 http://www.sheepusa.org/index.phtml?page=site/text&nav_id=3c081c2af5f98f1a054911 d06824094f.

124 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES with the producer about biosecurity practices, as well as a review of vaccina- tion 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 com- mingling new animals with the existing flock. Contact with other sheep dur- ing 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 addi- tions 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-re- lated 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 com- mon 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:

SHEEP HEALTH ISSUES 125 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 transmis- sion 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 nec- rophorum, which is present in the environment, assists Dichelobacter (for- merly 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, trim- ming of the feet, and rigorous culling, as well as determination and dedica- tion 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 re- spiratory 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

126 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES 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 pre- mature 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, consider- able 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 pap- ules 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).

SHEEP HEALTH ISSUES 127 Caseous Lymphadenitis (CL) Caseous lymphadenitis (CL) can be of considerable economic impor- tance 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 usu- ally 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 con- tains 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.” Broncho- pneumonia, 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. Ani- mals 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 paratubur- culosis, 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 implica- tions for sheep exported from the United States. The disease is discussed in greater detail in sections below.

128 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES Ram Epididymitis (RE) Ram epididymitis is more common in western range flocks and com- monly 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 re- cords, 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 produc- ers 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 pa- rameters 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,

SHEEP HEALTH ISSUES 129 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, measur- ing 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 per- cent 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 identifica- tion 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 Scra- pie 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-

130 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES fied to the flock of origin (flock in which an animal most recently resided for breeding). Animals required to be officially identified include: a. All breeding sheep; b. All sexually intact animals for exhibition; c. All sheep over 18 months of age; d. 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; e. All suspect and test-positive animals; f. Animals from noncompliant flocks; g. Breeding goats, except low-risk commercial goats. Animals not required to be individually identified include: a. 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); b. Wethers for exhibition and wethers under 18 months of age; c. Slaughter goats (goats in slaughter channels); d. Low-risk commercial goats; e. Animals shipped directly to an approved slaughter facility or an ap- proved 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); f. 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 iden- tification 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

SHEEP HEALTH ISSUES 131 extent, this is what happened in the cattle industry where identification was linked to the brucellosis program. As brucellosis was eliminated, identifica- tion 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 re- quirements. 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‑ap- proved ID such as an official eartag: 1. All animals one year of age or older; 2. All acquired animals before commingling with the flock unless al- ready identified with an approved device; and 3. 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 me- dia reaction subsided, certain livestock species groups began to withdraw support for a mandatory identification program and urged the U.S. Depart- ment of Agriculture (USDA) to implement a voluntary national identifica- tion 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 regis- ter 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

132 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES premise identification number that corresponds to the contact information provided. The identification component provides the owner with a nationally unique identification for the animals on a registered premise. The identifi- cation number stays with individual animals (animal identification number [AIN]) or with lots or groups of animals (group identification number [GIN]) throughout their lifetime. This number links the animal to its birthplace or premises of origin. When combined with animal tracing, the AIN/GIN also links the animal to each premises or location that has been reported for it. The federal government, states, and industry groups actively encourage producers to at least register their premises. To accomplish the goal of a 48‑hour trace, a high rate of voluntary participation in NAIS will be neces- sary. Sheep identification requirements for scrapie are currently accepted as meeting the NAIS goal of enhancing animal traceability. By developing consistent standards for the official identification of livestock species across USDA Animal and Plant Health Inspection Service (APHIS) programs, NAIS supports USDA and the industry’s long‑term goal of enhancing international trade and marketing opportunities. The Sheep Working Group of NAIS (NAIS, 2006) recommended that: • The existing mandatory identification should be used as a start- ing point for NAIS as it is more complete than what exists for any other species. • The Working Group acknowledges that a purely visual identification system will not work to attain the goal of tracing within 48 hours and an electronic system is needed. However, a proven system of electronic identi- fication and tracking does not exist for small ruminants. • USDA should conduct research to develop an electronic system or test systems developed in other countries. Educational Resources To educate themselves on various issues regarding sheep production in- cluding animal health, producers utilize a multitude of resources. According to the 1996 NAHMS survey (USDA, 1996), the following are the top 10 resources used by producers, with the percentage of sheep operations that use the associated resource in parentheses: Magazines/newsletters (70.5) Neighbors/other sheep producers (69.4) Use of a veterinarian (63.3) Other books (50.5)

SHEEP HEALTH ISSUES 133 Shearer (49.5) University/Extension (49.2) Fairs and shows (42.3) Meetings (35.4) Feed and drug salespersons (26.5) Sheep Industry Development (SID) Sheep Production Handbook (24.1) In the 2001 NAHMS survey (USDA, 2002), producers were asked what sources of information are important. Their top responses and the percentage of operations reporting that the resource is very important are as follows: 1. Veterinarians, private practitioners, consultants (39.1) 2. Other sheep producers (30.0) 3. Shearers (29.3) 4. Magazines, newsletters (22.7) 5. University/Extension (22.0) 6. SID handbook (10.5) 7. Meetings (10.2) 8. Feed and drug salespersons (9.2) 9. Internet (7.3) In the 1996 study, more than 35 percent of the operations did not list veterinarians as a source of sheep information (USDA, 1996). In the 2001 study, only 39.1 percent of all sheep operations reported that veterinarians are a very important source of sheep health information and 27.9 percent of operations listed veterinarians as not important (USDA, 2002). In 2000, 46.1 percent of sheep operations consulted a veterinarian. Past NAHMS studies of other species revealed a significantly different picture. The percentages of operations involving other species that consulted a vet- erinarian were as follows (USDA, 2002): • Swine (2000) — 78 percent • Equine (1998) — 73.8 percent • Dairy (1996) — 98.1 percent • Feedlot (1999) — 97.4 percent • Beef (1997) — 55 percent Exploring this subject further may shed light on reasons for the differ- ence between sheep and most other species. There do not appear to be data on whether producers feel they have sufficient information and assistance on prevention and control of disease, lambing issues, or nutritional problems. Do many sheep producers not use the services of veterinarians because of the

134 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES lack of availability, lack of knowledge about sheep, cost, fewer disease and health issues, or something else? Would the increased use of veterinarians and veterinary services provide a benefit and added value or merely add a cost without adequate return? Commonly accepted anecdotal information suggests that there is a shortage of veterinarians whose practices include small ruminant medicine or who are knowledgeable about sheep. In recent years, there has been a growing concern within the veterinary profession about a shortage of veteri- narians in the area of food supply veterinary medicine (FSVM). The FSVM specialty includes private practice serving dairy, beef, swine, poultry, sheep, and goat operations, as well as federal and state animal health officials in- volved with food safety and animal health. The American Veterinary Medi- cal Association (AVMA) and other organizations have studied the potential problem of shortages within FSVM. A study published in 1999 predicted that there would be a decrease in the demand for large-animal practitioners (Brown and Silverman, 1999). A 13‑panel Delphi study published in 2006 found that FSVM will face opportunities and challenges. This study confirmed the anecdotal informa- tion and conflicted with the 1999 report. A key finding was a predicted shortage of food supply veterinarians. Interestingly, both the poultry and small ruminant panels predicted a close match between supply and demand. However, the small ruminant panel predicted a slight shortage of practitio- ners (Prince et al., 2006). A 2007 ASI policy resolution declared that the U.S. sheep industry is in need of qualified veterinarians with knowledge of sheep diseases and management practices. The ASI supports a curriculum that includes an emphasis on related sheep diseases and applied sheep health management practices. The real problem may well be that there has been a shortage of knowledgeable and experienced veterinarians willing to do small ruminant work over such an extended period of time that the industry has found ways to manage without veterinarians. Sheep Disease Pharmaceuticals In the United States, there is a critical shortage of approved animal drugs intended for less common animal species (minor species) or a ma- jor species such as cattle suffering from an uncommon condition. Sheep and goats are considered minor species. Few animal drugs are specifically approved for sheep and goats. Consequently, veterinarians and livestock producers often have limited options for treating sheep if they become ill. The shortage of approved drugs may result in animal suffering, increased mortality, and financial loss to those who raise the animals. Congress recognized that statutory changes might be needed to address the described shortage of approved animal drugs in the Animal Drug Avail-

SHEEP HEALTH ISSUES 135 ability Act (ADAA) (P.L. 104-250), passed in 1993 (see Chapter 2 for a fur- ther discussion of this federal policy). A section of the legislation recognized particular problems relating to the availability of approved animal drugs for minor uses in major species and for use in minor species. The law directed the Secretary of Health and Human Services to consider and announce pro- posals for legislative or regulatory change to the approval process for such drugs. The Food and Drug Administration (FDA) concluded that federal statutes should be amended. The FDA proposals provide the conceptual base for the Minor Use and Minor Species Animal Health Act of 2001. The Minor Use and Minor Species (MUMS) Animal Health Act of 2001 is similar to the Human Orphan Drug Act of 1983. This act is intended as a mechanism to provide FDA-authorized drugs for less common animal species and health indications. Specifically, MUMS seeks to provide labeled drugs for needy minor species, including sheep, goats, game birds, emus, ranched deer, alpacas, llamas, deer, elk, rabbits, guinea pigs, pet birds, reptiles, ornamental and other fish, shellfish, wildlife, and zoo and aquaria animals. The MUMS Act is also designed to provide major species (cats, dogs, horses, cattle, swine, turkey, chickens) with needed therapeutics for uncommon indications, so‑called minor uses. Despite MUMS, however, there is still a shortage of therapeutics for sheep. For example, there is a tremendous need for additional deworm- ers as internal parasites have developed a resistance to the drugs currently available (see further discussion below). The ASI supports legislative and regulatory efforts that will restructure and expedite the drug approval pro- cess while maintaining product safety and efficacy. DISEASES OF ECONOMIC IMPACT OR CONCERN The two NAHMS studies (USDA, 1996, 2002) provide data on diseases that are present and are of concern to the sheep industry. Many of the condi- tions identified as of high or moderate concern, such as intestinal parasites, contagious ecthyma (soremouth), foot rot, and mastitis, are not usually fatal if the animals receive proper treatment. Nevertheless, these conditions are insidious and debilitating, affect production efficiency, and add to produc- tion costs. Unfortunately, there are no hard data as to the actual costs of the diseases, which would include production losses, treatments, and mor- talities. Data regarding actual costs are essential to set priorities and make educated decisions on research, prevention, and control needs. The most commonly reported disease or condition of concern in the 1996 NAHMS study was stomach/intestinal worms, reported to be of moderate or high concern by 62.1 percent of sheep operations (Figure 3-1). Nearly half of all operations surveyed reported problems with stomach/in- testinal worms in the previous 5 years (Figure 3-2). In the 2001 NAHMS

136 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES Stomach/Intestinal worms 62.1 Mastitis 42.7 Footrot 40.5 Vit. E/Selenium deficiency 35.7 Scours 34.9 Coccidiosis 31.7 Pregnancy disease (toxemia) 31.4 Pasturella pneumonia 25.9 Sore mouth (Orf) 25.7 Clostridial diseases 24.5 Grain overload 24.5 Keds (sheep ticks) 23.8 23.5 Liver flukes 20.3 Lice 19.9 Campylobacter (vibrio abortion) 0 10 20 30 40 50 60 70 Percent Operations FIGURE 3-1  Percent of operations that reported moderate or high concern for the top 15 conditions of concern. Source: Reproduced from USDA (1996a). 3-1 new.eps Stomach/Intestinal worms 48.6 Mastitis 37.5 Footrot 28.1 Scours 27.5 Sore mouth (Orf) 20.6 Vit. E/Selenium deficiency 20.1 Pregnancy disease (toxemia) 19.2 Keds (sheep ticks) 19.1 Coccidiosis 18.2 Grain overload (rumen acidosis) 15.3 Pasturella pneumonia 13.8 Caseous lymphadentis 13.8 Bad teeth 13.6 Lice 12.2 Fly strike 10.7 0 10 20 30 40 50 60 Percent Operations FIGURE 3-2  Percent of operations on which the top 15 conditions of concern were known to be present in the last 5 years. Source: Reproduced from USDA (1996a). 3-2 new.eps

SHEEP HEALTH ISSUES 137 study, 74 percent of sheep operations reported the presence of stomach or intestinal worms in the previous three years (Figure 3-3). Although the purpose of this section is not to provide a technical review of the common diseases, it examines intestinal parasites as an example of the need for economic and other data. The most common internal parasites affecting sheep throughout the United States are roundworms or nema- todes. The gastrointestinal nematodes of greatest importance in sheep are members of the order Strongylida and include Haemonchus, Teladorsagia, Trichostrongylus, Cooperia, and Nematodirus. These species have a direct life cycle, meaning that sheep are the only host. Adult worms in the gastro- intestinal tract of sheep lay eggs that are passed in the feces and contaminate the environment. When conditions are suitable, the eggs hatch into a larval stage that matures. The first two larval stages are nonparasitic but the third stage is infective. Part of the parasite maturation process takes place on the pasture and part within the abomasum (stomach) or small intestine of the sheep. Sheep that graze an infected pasture ingest the third‑stage larva, which finishes development into egg-laying adult worms. During periods where environmental conditions are harsh, the parasite larvae in the stomach undergo a process called hypobiosis, which means their development is delayed. The delay extends until pasture conditions are favorable for survival of the parasite. Over time, sheep may develop some resistance to these worms. The development of resistance is complex and involves genetic components. Lambs are extremely susceptible as are older Johne’s 1.6 Scrapie 1.2 OPP 7.1 Footrot 34.9 Lumpy jaw 20.4 Stomach or intestinal worms 74.0 Enterotoxemia/overeating 38.8 Other clostridial disease 11.9 Coccidiosis 30.4 Sore mouth 40.0 Ring worm or club lamb fungus 7.3 Bluetongue 4.2 0 10 20 30 40 50 60 70 Percent FIGURE 3-3  Percent of operations where diseases were present (suspected or confirmed) during the last 3 years. Source: Reproduced from USDA (2003a). The survey was completed in early 2001. 3-3 new.pdf

138 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES sheep that have compromised immune systems from other diseases, from poor nutrition, or during lambing. Ewes usually experience a temporary relaxation of immunity slightly before and after lambing. Infected ewes may shed large numbers of worm eggs into the environment that develop into larvae and are ingested by the lambs. The overall effect of internal parasites is known as parasitic gastroenteri- tis. Clinically, symptoms of internal parasitism may be insidious at the onset. Infected lambs grow more slowly and become unthrifty, food intake is often reduced, and, if the lamb is left untreated, it may die. Larger worm burdens may result in higher lamb mortalities. Clinical disease is not restricted to lambs. Adult sheep already in poor condition, stressed by milk production, or with existing disease conditions may also suffer clinical manifestations such as weight loss, reduced milk production, and even death. Haemonchus contortus, the barberpole or wireworm can be particularly severe. The fourth‑stage larva and adult Haemonchus are known to be vig- orous bloodsuckers. The worms can deplete volumes of blood large enough to result in anemia and death. H. contortus is very prolific and a female may produce thousands of eggs each day, which may then contaminate grazing pastures. Unlike the other gastrointestinal parasites, sheep burdened with H. contortus do not usually have diarrhea as a primary sign, thus owners may not appreciate the extent of the infection until it is too late to save the animal (Zajac, 2006). Damage caused by Teladorsagia circumcincta (formerly called Osterta- gia circumcincta) is targeted at the abomasal gastric glands. Heavy infection with T. circumcincta can cause diarrhea, and hypoproteinemia, which may result in death. More commonly, moderate infections cause diarrhea with poor weight gain or weight loss (Zajac, 2006). In the United States, the third common nematode group to contribute to parasitic gastroenteritis is Trichostrongylus. Severe infections of Tricho- strongylus can result in diarrhea and weight loss (Zajac, 2006). There have been two human infections of Trichostrongylus reported in Australia. Vegetables grown using fresh goat manure as fertilizer were eaten raw and apparently transmitted Trichostrongylus (Ralph et al., 2006). Drugs used to treat internal parasites in sheep are called anthelmintics. The anthelmintics available in the United States belong to three major chemical classes. These are: • Benzimidazoles—albendazole and fenbendazole are sold in the United States for small ruminants. Albendazole is labeled for sheep but not goats, and fenbendazole is not labeled for sheep. • Macrocyclic lactones—ivermectin and moxidectin are approved for oral use in sheep. Currently ivermectin is the only anthelmintic approved for limited use in nonslaughter organically raised sheep in the United States.

SHEEP HEALTH ISSUES 139 • Nicotinic anthelmintics—this group includes levamisole, morantel, and pyrantel. Only levamisole is approved for sheep. The limited availability of anthelmintics for sheep is significant because internal parasites have developed, or have begun to develop, resistance to the treatments. Some of the past treatment regimens actually assisted the development of anthelmintic resistance. Failure of the overall parasite con- trol program on sheep operations is often due to mismanagement (Radostits et al., 2007). A proportion of all worm populations have the genetic capacity for resistance to some or all classes of anthelmintics. This allows their survival when others die. Frequent use of anthelmintics as the major way of con- trolling parasites has allowed the development of resistant populations that have become a major problem, especially in the South. Although frequent use of anthelmintics is perhaps the major selection force for the development of resistance, underdosing a treatment also provides a powerful selection mechanism. When a population of worms becomes resistant to one member of a class of drugs, it effectively becomes resistant to other members of that class. Unfortunately, when resistance of a worm population to an anthelmin- tic becomes evident, it will likely remain even if the use of that compound is discontinued for several years. Resistant worms can be introduced onto a new farm with the introduction of new animals (Craig, 2006). Current treatment strategies to increase the efficacy of the anthelmintics involve the judicious use of drugs combined with pasture management and monitoring the sheep for fecal egg counts and other disease indicators, such as anemia. A summary is provided by Craig (2006): • Delivery of treatment—dividing the dose of an anthelmintic over several days or fasting the animal before treatment may enhance the effectiveness. • Use of drug combinations—this may be the only choice in places where resistance to multiple classes of anthelmintic has developed. Although certain drugs may not be effective on their own, these may work in combina- tion with others. They should be used at full dosage and concurrently. • Drug rotations—the practice of changing drugs within a grazing season actually selects for resistance to all the drugs used and can accelerate the process of resistance. • Targeted or selective treatment—this approach involves treating only sheep with signs of disease (e.g., high egg counts or pale mucous mem- branes). The untreated animals will carry worms that are susceptible to treatment. Worms that are not treated are called “in refugia.” Having some worms in refugia (not exposed to an anthelmintic) slows the development of resistance by diluting the frequency of resistant genes. Consequently, when a

140 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES dewormer is required, it will be effective because the worms will be suscep- tible to treatment (Kaplan, 2004). The FAMACHA system uses a patented color chart to allow producers to identify animals with moderate or severe anemia (H. contortus infections) for treatment, leaving up to 80 percent of the animals untreated. Other strategies include only treating thin animals or leaving 10–20 percent of a group untreated when changing pastures to maintain a level of “refugia.” • Culling of more susceptible animals—certain sheep may consistently have high fecal egg counts or clinical signs of parasitism. Culling these animals can improve the overall resistance of the flock (Barger and Dash, 1987). • Use of breeds that show resistance to parasites—some breeds have a degree of genetic resistance to parasites and may carry a smaller worm burden. It is possible to identify these animals and select for a flock carry- ing a higher level of resistance to parasitism. However, even in these breeds there are differences among individual animals that influence the course of disease. • Pasture management practices—pasture rotation, alternative grazing or cograzing with different species such as cattle or horses, or using pas- tures that have been cropped may lower the worm burden when sheep are returned to the pastures. • Nontraditional treatments—the use of copper oxide wire particles or certain botanical products may be useful alternatives to anthelminthics, but most need more scientific scrutiny before they can be adapted for wide- spread use. As discussed above, the newer control strategies require a more detailed level of sheep and pasture management. There are no data that capture the total economic loss to the sheep industry because of internal parasites despite it being the disease condition of highest concern and highest reported incidence. Such data are important as they could be used to encourage research for additional control measures that may include the development of new anthelmintics and evaluating the effectiveness of other management practices. Inadequate data is a problem for most other sheep disease conditions such as mastitis, foot rot, and Johne’s disease, not just internal parasites. Causes of Death A USDA (2005) study by APHIS examined the nonpredator causes of death for lambs and adult sheep in the United States. Since 1994, nonpreda- tor causes of death have been responsible for 62 percent of lamb and adult sheep losses, more than from predators nationally and in all regions of the

SHEEP HEALTH ISSUES 141 country. In the 2004 NAHMS study of mature sheep losses, old age was reported as the leading cause of death (26.8 percent of adult sheep death loss) followed by lambing problems (13.4 percent); digestive problems such as internal parasites, bloat, scours, and acidosis (12.9 percent); and cause unknown (12.1 percent). The primary nonpredator causes of death in lambs were respiratory problems such as pneumonia, and shipping fever (22.8 percent); digestive problems, such as internal parasites, bloat, scours, and acidosis (19.8 percent); weather-related causes such as chilling, drowning, and lightning (14.8 percent); lambing problems (14.7 percent); and cause unknown (13.3 percent). Loss estimates for the Pacific (California, Oregon, and Washington) and West Central (Arizona, Colorado, Idaho, Montana, New Mexico, Nevada, Texas, Utah, and Wyoming) regions were made after docking, marking, or branding, while estimates for the Central, Northeast, and Southeast regions were made from birth. In fact, in the western states, the National Agricultural Statistics Service (NASS) defines lamb crop as those lambs marked, docked, or branded. The exclusion of predocking losses from these regions is because lambs are usually born on the range and less likely to be counted. Five states conduct surveys that include these early losses: Colorado, Idaho, Montana, Utah, and Wyoming. Other than Colorado, which shows predocking losses at 32 percent of all lamb losses, the other four states report predocking lamb losses over 50 percent of all lamb losses. (USDA, 2005). The lack of data regarding lamb numbers during the predocking period in states that have some of the highest sheep numbers is significant. An ac- curate estimate of the actual lamb crop in the United States cannot be de- veloped without death loss data for the predocking period. More important, efforts to reduce such losses are encumbered without an accurate baseline that could provide answers to various questions 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 insufficient colostrum or poor mothering? • Are lambs dying at a few weeks of age from scours, pneumonia, or other reasons? • Are predators responsible for the majority of deaths? Scrapie As a disease entity for individual flock owners in the United States, scrapie did not make the list of the top 15 conditions of moderate or high

142 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES concern in the 1996 NAHMS study (USDA, 1996), but it is the only sheep disease that has had a congressionally funded program aimed at control and/ or eradication since 1952. In fact, federal regulations mandating an acceler- ated scrapie eradication program went into effect in 2001. When publishing this proposed rule, APHIS estimated that it would cost approximately $100 million over 7 years to accomplish the task of eliminating scrapie outbreaks (Federal Register, 2001). During the 1980s, scrapie was considered “a minor disease in a minor species.” In 1987–1988, APHIS published a proposed rule asking for com- ments on whether to discontinue the scrapie program. The publication of the proposed rule came shortly after the United Kingdom’s announcement that it had identified a new disease entity that affected cattle and appeared to be re- lated to scrapie. Comments on the proposed rule overwhelmingly requested that APHIS not discontinue the scrapie program but work together with the sheep and allied industries to develop a new program. Many comments cited BSE as the reason for a renewed interest in control. In 1990, the spread of BSE to other species, including cats, highlighted the hidden dangers associ- ated with these diseases. A new program was developed through the process of negotiated rulemaking and went into effect in 1992. The new program was multifaceted in that it consisted of the establishment of a national scra- pie flock certification program (SFCP) and interstate regulations to identify and restrict the movement of certain sheep from scrapie-infected and source flocks. The basis of the certification program is to provide a source of sheep having a negligible risk of scrapie (Detwiler et al., 1997). The foundation of this program is still in effect although it has been modified based on new scientific findings. As stated above, there is a concerted effort to eliminate scrapie from the United States by 2010. The UK announcement in 1996 that 10 deaths (adolescents and young adults) were thought to be attributed to BSE brought the transmissible spongiform encephalopathies (TSE) to the world’s center stage. Classical Scrapie Scrapie is an insidious, degenerative disease affecting the central nervous system of sheep, goats, and moufflon. The disease is also called La trem- blante (French: trembling), Traberkrankheit (German: trotting disease), or Rida (Icelandic: ataxia or tremor). Scrapie has been reported worldwide and affects most sheep-producing regions with few notable exceptions. Australia and New Zealand are commonly accepted to be scrapie free. The disease has been recognized for over two centuries in England, Wales, and Germany (Parry, 1983). Scrapie is the prototype of the group of the TSE diseases. Other TSE in- clude Creutzfeldt-Jakob disease (CJD), kuru, Gerstmann-Sträussler-Scheink-

SHEEP HEALTH ISSUES 143 er disease (GSS), fatal familial insomnia (FFI), and variant Creutzfeldt-Jakob disease (vCJD) in humans and transmissible mink encephalopathy (TME), chronic wasting disease (CWD), bovine spongiform encephalopathy (BSE), atypical BSE, BSE in a goat (Eloit et al., 2005), feline spongiform encepha- lopathy (FSE), and atypical scrapie in sheep. These diseases are caused by transmissible agents yet to be fully characterized, all of which share a num- ber of common characteristics: • Prolonged incubation period of months or years; • Progressive debilitating neurological illness that appears to always be fatal; • Pathological changes confined to the central nervous system (CNS); and • The transmissible agent elicits no detectable specific immune re- sponse in the host, which has inhibited the development of a live animal diagnostic test and vaccines. The clinical disease occurs primarily in sheep of breeding age because the minimum incubation period is usually between 18 and 24 months. Scrapie occurs most frequently in sheep of either sex between 2 and 5 years of age. Although cases of the disease are not common before 18 months, a few cases of natural scrapie have been reported in sheep at approximately 1 year of age and it may occur in animals over 5 years of age (Detwiler and Baylis, 2003). Sheep usually become exposed to scrapie through an oral route. Once the agent enters the body, it replicates and infects most tissues, including ton- sils, spleen, lymph nodes, brain, and spinal cord (Hadlow et al., 1979, 1982; van Keulen et al., 1996, 1999); blood (Hunter et al., 2002); and peripheral nerves (Groschup et al., 1996). There is also evidence that scrapie‑infected sheep may harbor infectivity in actual muscle cells apart from the peripheral nerves (Pattison and Millson, 1962; Andréoletti et al., 2004; Casalone et al., 2005). In the past, milk had not been considered a risk factor for scrapie. However, in 2005, a published study began to suggest milk as a possible route of transmission. This research found that sheep concurrently infected with scrapie and a chronic inflammatory disease such as OPP have prions in the mammary gland and may shed these into milk (Ligios et al., 2005). Recently, it was found that lambs fed milk from scrapie-affected ewes be- came infected with scrapie (Konold et al., 2008). Certain sheep may shed the scrapie agent via the placenta and likely the birthing fluids. Thus, scrapie is thought to spread from an infected ewe at or near the time of lambing to susceptible lambs or other susceptible sheep that may be exposed to the placenta (see Pattison et al., 1972, 1974; Onodera et al., 1993; Race et al., 1998).

144 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES Over the decades, there has been debate about the nature of scrapie and whether it is a genetic disease or is transmitted between sheep (Dick- inson et al., 1974; Parry, 1983). Research in the 1990s found that scrapie was influenced by genetics, specifically the sequence of the gene coding for prion protein (Westaway et al., 1994; Hunter et al., 1994, 1996; Hunter, 1997). There is also evidence indicating that scrapie is not a genetic disease (Hunter et al., 1997). Most classical scrapie cases have historically been found in sheep carrying the VRQ and ARQ alleles, and it was thought that sheep having two ARR alleles were resistant to scrapie. Consequently, many countries shifted their scrapie control program to a genetics-based program or at least included a genetic (breeding) component (Detwiler and Baylis, 2003). Newer diagnostics as well as extensive testing programs in Europe have begun to call into question whether there truly are genotypes that are fully resistant to TSE infection (Buschmann et al., 2004; Le Dur et al., 2005; Groschup et al., 2007). There have been many different approaches to scrapie control and eradi- cation. Countries such as Australia and New Zealand, which have detected the disease after introduction but before widespread transmission, have apparently been successful in eradicating the disease within a short period of time. Other countries, in which the disease has become endemic, such as Canada, Iceland, and the United States, have implemented various strategies in an effort to eliminate the disease. The emergence of BSE in 1986 and the experimental transmission of BSE to sheep and goats have been the impetus for a significant increase in research and have prompted a number of other scrapie-endemic regions such as the European Union to initiate programs to eliminate the disease The United States has tried many options to eradicate scrapie (see the Appendix for a chronology of U.S. control efforts). Historically, none has been very successful, which may be attributed to a number of factors. First and foremost, the lack of scientific advancements, especially in the area of preclinical diagnostics and understanding the exact nature of the patho- genesis, has hampered control programs. For example, when during the incubation period an animal starts to shed the agent and by what route(s) are not known. Such information is necessary to identify animals that may be exposed. All of the tests have limitations. None have adequate sensitivity to be able to declare an individual animal free of scrapie (O’Rourke et al., 2000; González et al., 2005). Only recently have live animal tests become available to diagnose an infected animal before the onset of signs, which is usually years after the animal has become infected and may be a risk to other sheep. Despite some of these limitations, recent scientific advancements have finally provided the necessary tools for the current control program to demonstrate that its measures have resulted in a decrease in the prevalence of classical scrapie.

SHEEP HEALTH ISSUES 145 The properties of the causative agent are unusual because it is able to survive conditions that normally destroy other agents such as bacteria and viruses. The causative agent can survive conditions such as boiling, dry heat up to 600°C, formalin fixation, and treatments with many common disinfectants (WHO, 1999). The trait of survivability also allows the agent to remain in the environment for extended periods of time. How long the agent may persist and pose a risk to other animals if shed into the environ- ment is unknown. Two different studies have shown that scrapie infectivity can survive in the environment at least 2–3 years and possibly a great deal longer (Brown and Gajdusek, 1991; Seidel et al., 2007). The most recent studies have demonstrated infectivity not only in the soil itself, but also in the aqueous soil extract (Seidel et al., 2007). Despite more than 250 years of potential for human exposure to scra- pie, there is no scientific evidence to date indicating that scrapie poses a public health risk (Harries Jones et al., 1988). During a consultation held in 1999, the World Health Organization reviewed existing evidence, includ- ing a 15‑year epidemiological study (Brown et al., 1987), and came to the same conclusion (WHO, 1999). Nevertheless, with the detection of atypical manifestations of certain TSE such as scrapie and BSE, public health of- ficials must remain vigilant for any potential change in virulence and host susceptibility. Prevalence of Classical Scrapie Before the Scrapie Ovine Slaughter Surveillance (SOSS) study, the es- timated prevalence of scrapie in the United States was 0.07 percent. How- ever, this estimate was based on results obtained from the 1996 NAHMS sheep study, which relied on data from a producer-generated mail-in survey (USDA, 2003d,e). The prevalence in this study was estimated from those producers reporting confirmed or suspected scrapie in their flocks over a period of 5 years. More recently, estimates of prevalence derived from the results of the SOSS study were actually based on positive tests. The vast differences between the methodologies of the NAHMS and SOSS studies prevent any accurate comparison. Of the 12,508 samples collected in the SOSS study, 12,491 valid test results were obtained (99.9 percent). The study concluded that the overall weighted national prevalence of scrapie in mature sheep was 0.20 percent. On a regional basis, scrapie was found to be most prevalent in the Eastern (0.52 percent), followed by the Central (0.21 percent) and Mountain (0.14 percent) regions (Figure 3-4). Even though the small sample size from the Western region prohibited an estimate for the region itself, the results for the region were included in the national estimate (USDA, 2003d,e).

146 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES West Mountain Central East Percent Region FIGURE 3-4 Percent of that sheep tested positive for scrapie by region. Note: Because of the low number of samples obtained in the Western region, results for the Western region are included in the national estimates but are not listed individually. Source: Reproduced from USDA (2003d).new.pdf were collected between April 1, 3-4 Samples 2002, and March 31, 2003. About 84 percent of the positive samples were from black-faced sheep and less than 0.01 percent from white-faced sheep. Mottled‑faced sheep represented 0.12 percent of the positives (USDA, 2003d,e). The breed results are similar to those that have been obtained over the years through passive surveillance. The study found that black-faced sheep were significantly more likely to test positive even when adjusting for other factors. The fact that scrapie appears to be predominant mostly in black-faced and mottled-faced sheep and extremely limited in white-faced sheep is important because the majority of sheep (67 percent) in the United States are white-faced (USDA, 1996). All of the sheep that tested positive were homozygous for glutamine (QQ) at codon 171. This genotype has been characterized as one of the most susceptible for classical scrapie (USDA, 2003d,e). Current Scrapie Program The current National Scrapie Eradication Program (NSEP) is comprised of active testing of targeted mature sheep and goats at slaughter with trace- back of positive animals to the flock of origin. Additional infected flocks are identified by tracing exposed animals out of these flocks. Effective tracing

SHEEP HEALTH ISSUES 147 can be done as a result of the identification requirements implemented in 2001. As infected or source flocks are identified, government veterinarians work with producers to develop a plan to remove animals determined to be most susceptible. In addition, the premise may have to be cleaned and disinfected. Most flocks use a genetics-based plan to clean up. Indemnity funds are available for animals that must be removed to comply with the clean-up plan. In addition, those exposed animals that have been sold from the flock will be traced and tested if still alive. There are three basic steps in the current NSEP: 1. When an infected flock has been identified, the sheep are genotyped to determine disease risk. 2. Susceptible genotypes are either removed or their movement restricted. 3. The identified flock is placed under surveillance for 5 years. In most cases, producers will be able to keep many more of their sheep with the genetics-based plan. This plan allows owners to retain or sell without restrictions nearly all sheep that are AA RR, AA QR, and most AV QR from infected or source flocks once owners have met certain conditions (see NIAA, 2003, for more details). On average, an estimated 60 percent of a flock can be preserved when using a genetics-based plan compared to 25 percent when using a traditional plan. Another component of the scrapie eradication effort is the Scrapie Flock Certification Program (SFCP). Given that the live animal testing for scra- pie cannot yet guarantee absence of scrapie infectivity, the SFCP monitors flocks over time and confers a certified status on those animals that do not have evidence of the disease after a minimum of five years of complying with movement, identification, recordkeeping, and sampling requirements. The basis of this program is to provide a source of sheep that would have a negligible risk for having scrapie. Most important, the accelerated eradication program requires an iden- tification and recordkeeping system, which allows diseased, exposed, and high-risk animals to be traced back to their flock/herd of origin so that the spread of scrapie within and from these flocks/herds can be prevented. The scrapie eradication regulations published in 2001 also established a pro- gram to recognize states that conducted an active scrapie control program consistent with federal requirements. Additional restrictions were placed on the movement of sheep from states that do not require that scrapie be a reportable disease and/or do not quarantine infected and source flocks. Congressional funding for the NSEP has increased from $15 million in 2003 to $18.4 million in 2007. When publishing the proposed rule in 2000, APHIS estimated the total cost to eradicate scrapie over a 7‑year period

148 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES to be 100 million dollars (USDA, 2000). In a letter to Undersecretary of Agriculture Bruce Knight, ASI requested that the USDA increase its scrapie budget request to $28.6 million for fiscal year 2009. In Fiscal Year (FY) 2006, the NSEP made significant progress as shown by the reduction in the percentage of sheep of all face colors that tested posi- tive at slaughter and the decrease in the number of positive animals found at slaughter. The result was fewer newly infected and source flocks and fewer animals indemnified in comparison to FY 2005. For example, the number of scrapie‑positive, black‑faced sheep dropped from slightly under 0.9 percent in FY 2004 to < 0.5 percent in FY 2006 (USDA, 2007a). Economic and Trade Effects of Scrapie The USDA has estimated that producers annually incur losses of $20 million from scrapie (USDA, 2000). The costs are associated with decreased productivity of infected flocks, diminished potential for exports (live ani- mals, germplasm, and byproducts), and increased costs of disposal (USDA, 2000). Because scrapie is always fatal, there are two considerations when ex- amining the direct economic impact of scrapie on domestic flocks. These are the overall prevalence of the disease across all U.S. flocks and the within-flock prevalence of infected flocks. The overall weighted prevalence of scrapie in the United States (0.20 percent) is low, especially when com- pared to diseases such as OPP which had a seroprevalence calculated at 24.2 percent. Seroprevalence of OPP was measured during the 2001 NAHMS sheep study by testing sheep on randomly selected sheep operations. Over 21,000 samples collected at 682 operations that agreed to participate were tested. Overall, 36.4 percent of the operations had one or more positive animals (USDA, 2003c). Although uncommon, flocks heavily infected with scrapie and that contain a high percentage of susceptible animals may experience significant mortality losses. In flocks where scrapie is endemic, the number of infected animals increases and the age at onset of clinical signs decreases over a period of several years making these flocks economically unviable. Surveys of farmers in Great Britain and the Netherlands have found mean within- flock incidences of 0.37 percent and 1.2 percent, respectively (Schreuder et al., 1993; Hoinville et al., 2000). Other observations have included within- flock incidences ranging from 1 percent to 20 percent (Young et al., 1964; Sigurdarson, 1991; Hoinville et al., 2000). With the promotion of breeding programs that protect sheep from the clinical signs and subsequent death from scrapie, most U.S. sheep producers are not likely to experience a significant within-flock incidence. Hence, for many U.S. producers, the direct animal losses from scrapie may be insignifi-

SHEEP HEALTH ISSUES 149 cant. This conclusion is reflected in the 1996 NAHMS survey, which found that scrapie was not among the top 15 diseases of concern (USDA, 1996). The epidemiological finding that BSE was most likely spread by the feed- ing of ruminant meat and bone meal (MBM) to ruminants and the theory that the species of origin was sheep prompted voluntary action by U.S. renderers in the late 1980s. Many independent renderers imposed a volun- tary ban on the transportation and processing of sheep offal and/or heads, which had an impact on ovines slaughtered at small and very small packing plants. For those plants, the alternatives were to either send the head and offal back home with the producer or pass the cost of disposal back to the producer. If the producers had to dispose of the material themselves, the choices were to dispose of the materials on their own properties or through another mechanism such as a landfill at a cost. One study estimated that the costs for such disposal would average $150/ton (U.S. HHS, 1997). In that study, large lamb slaughterers were still able to use the byproducts for pet food. Another study reported value of the byproducts at $3.00 per carcass (Seitzinger et al., 2006). In 1997, the FDA enacted a regulation prohibiting the feeding of most mammalian protein (both cattle and sheep) to ruminants. The diversion of cattle offal created a separate stream for ruminant MBM in which sheep materials could be included without the extra costs of disposal. Sheep offal were then included with the bovine materials in meals to be fed to species such as pigs and poultry. This regulation actually assisted the sheep industry in that ovine offal could be combined with the larger pool of bovine offal and utilized, instead of having to be destroyed. Scrapie and BSE impact the trade of various sheep and lamb products including live animals, germplasm (semen and embryos), meat, and byprod- ucts such as MBM especially for pet food. Worldwide, only New Zealand and Australia are commonly recognized as scrapie‑free and, thus, are cur- rently the nations that can freely sell breeding stock to producers in most other countries. During the 1990s, actual statistics on the value of Austra- lian breeding stock sold indicates the amount was $29.2 million. The Terrestrial Animal Health Code (TAHC) of the World Organization for Animal Health (OIE) includes provisions to recognize a country free of scrapie, which would open up trade for the United States if the current eradication program is successful (OIE, 2007). The TAHC also includes provisions for individual flocks to be recognized scrapie‑free, thus allow- ing the export of breeding stock. As of June 2007, APHIS has modified the SFCP to allow for the monitoring and recognition of flocks to be certified for export, which will allow trade at least from some flocks without having the country declared scrapie‑free. The modifications for the export‑certified flock category are in accordance with the TAHC. Scrapie may also be a reason for regulatory restrictions on the export of

150 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES lamb MBM or the export of pet food to other countries. The actual value of the lost trade is not known and may not be significant. According to the Pet Food Institute, the U.S. supply and consistency of ovine MBM is not adequate to meet the demands of the domestic market so that supplemen- tal byproducts are imported from Australia and New Zealand (N. Cook, personal communication, 2007). Even if scrapie were to be eradicated im- mediately, restrictions on the trade of any ruminant MBM would still apply. As recommended by the TAHC, once a country has detected BSE in domestic cattle, other countries usually prohibit the importation of many ruminant products, especially ruminant MBM even for use in pet food (OIE, 2007). Scrapie is not the only disease that may impede or restrict the expor- tation of U.S. sheep to other countries. In addition, OPP, also known as Maedi-Visna, and ovine Johne’s disease (OJD) are both present in the U.S. sheep population. A number of countries have restrictions or requirements on imports of sheep from countries with these diseases. The TAHC includes a chapter on Maedi-Visna that outlines the provisions for trade. In addition to being recognized as scrapie‑free, both Australia and New Zealand have been recognized as free of OPP. Australia and New Zealand both have a control program for Johne’s disease (Seitzinger et al., 2006). Unlike scrapie, there are no U.S. government programs in place to eliminate or control OPP or OJD. A producer-driven effort to test for and control OPP is operated by the OPP Concerned Sheep Breeders Society. An attempt by the state of New Jersey to combine enrollment in the scrapie certification program and monitoring for OPP has been discontinued. Cur- rently, Minnesota has initiated a pilot program that combines monitoring for OPP with the scrapie certification program. Although there is a vol- untary control program for bovine Johne’s disease, there is no organized program for OJD. In 2006, USDA examined the market and economic effects of eliminat- ing scrapie alone versus eliminating scrapie, OPP, and OJD (Seitzinger et al., 2006). The study found that eliminating scrapie increased annual revenues to U.S. sheep and lamb producers by a total of $10.8 million dollars. The least increase in revenue from eliminating scrapie alone was from exports. The presence of OPP and OJD in the United States did not allow for a sig- nificant increase in revenue by the elimination of scrapie alone, as countries also have restrictions for OPP and OJD. Atypical Scrapie The term “atypical scrapie” has been adopted to describe forms of scrapie in which the findings in tested animals (including animals that ap- pear to be clinically normal) were different from those that were previously recognized as classical scrapie. Norwegian scientists published reports about

SHEEP HEALTH ISSUES 151 the first cases of nonclassical scrapie in 2003. They called this Nor 98 scrapie (Benestad et al., 2003). Hence, atypical scrapie cases are also called Nor 98 or Nor 98-like. Both types of scrapie (classical and atypical) involve the presence of abnormal prion protein. Most atypical cases differ from classical scrapie in that the lesions found in the brain as well as the deposits of prions have been concentrated mostly in the cerebrum and cerebellum rather than the brain stem. The patterns seen by Western Blot testing also differ from classical scrapie. �������������������������������������������������������������������� The average age of sheep with atypical scrapie is greater than that of classical scrapie. Research has found that over 58 percent of the cases of atypical scrapie in Germany were 6 years or older and 26.7 percent were older than 10 (���������������������� Lühken et al., 2007)��. Classical scrapie identified in clinically affected sheep usually occurs in certain genotypes of sheep. Most classical scrapie cases have traditionally been in sheep carrying the VRQ and ARQ alleles (homozygous or hetero- zygous), only occasionally in combination with ARR and AHQ. Atypical scrapie has been found predominantly in sheep carrying the AF141RQ, AHQ (Moum et al., 2005) ARQ, and ARR alleles. Atypical cases of scrapie have been found in ARR/ARR sheep in a number of European countries (European Union, 2006). Investigations of sheep that had difficulty walking (ataxia) led to the identification of Nor 98 scrapie in Norway, which was the first of the atypical scrapie variations to be characterized (Benestad et al., 2003). Subsequently, a number of countries have identified this type of scrapie or cases that have similar characteristics (De Brosschere et al., 2004; Gavier-Widen et al., 2004; Epstein et al., 2005). Before the fall of 2006, there had been no cases of a Nor 98-like scrapie found in U.S. sheep. When the SOSS study was conducted, a number of the characteristics associated with atypical scrapie had not been identified and some atypical cases of scrapie may have been missed. In November 2006, however, a sample was collected from an apparently healthy mottled-face sheep at slaughter (Wyoming Livestock Board, 2007). The characteristics found by the various diagnostic tests conducted revealed a Nor 98-like scrapie case. The sheep was traced back to a flock in Wyoming that was subsequently depopulated. Since then, four additional cases of Nor 98-like scrapie have been identified in the United States (USDA, 2007b). One of these cases of Nor 98-like scrapie (atypical) has been found in an ARR/ARR Suffolk sheep in the United States (D. Sutton, personal commu- nication, 2007). This case is significant because many countries, including the United States, have adopted control programs that promote breeding For more information, see the USDA information sheet “The Genetics of Scrapie Suscepti- bility” online at http://www.aphis.usda.gov/animal_health/animal_diseases/scrapie/downloads/ scrapie_genetics.pdf.

152 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES for ARR animals. These programs were initiated when it was thought that arginine (R) at codon 171 conferred complete resistance. There has been speculation that atypical scrapie may be a spontaneous disease, similar to CJD in humans. This theory has originated because most flocks have not been found to have additional cases (Hopp et al., 2006; Lühken et al., 2007). While a spontaneous origin is definitely a possibility, �������������������������������������������������������� if this “strain” of scrapie is predisposed to long incubation periods where sheep usually are culled or die from other causes, the disease may go unde- tected. The inability to diagnose such long incubation cases may lead to the conclusion that the disease is spontaneous. In regard to control programs, it will be important to determine whether the disease occurs sporadically or has a low rate of transmission. Many characteristics of “atypical” strains of scrapie are still unknown. For example, whether the disease transmits naturally from sheep to sheep is unknown, along with which tissues are infected and the potential host range. Research on these and other issues related to “atypical” scrapie is underway. The public health risk from atypical scrapie is also unknown. There is no basis for attributing a greater or lesser risk to humans from atypical scrapie than from BSE or classical scrapie. If atypical scrapie is not a new phenomenon and has simply been discovered recently, then the lack of epidemiological association between prion diseases in humans and sheep or in the consumption of sheep products suggests that atypical scrapie does not represent a risk to humans. This is not, however, a demonstration of absolute safety. In February 2007, the UK Chief Medical Officers sent a letter to neurologists to remind them to remain vigilant and refer unusual human neurological cases through the established national arrangements. The UK Spongiform Encephalopathy Advisory Committee (SEAC) considered the reminder important in part because of the unknown human health implica- tions of atypical scrapie (SEAC, 2007). Considerations for atypical scrapie include the following: • Monitoring of the epidemiological situation and related research to ensure timely and effective policy changes are made if needed; • Monitoring the occurrence of scrapie in the so-called “resistant” genotypes. If these genotypes have extended incubations or are subclinical carriers, the problem may go unnoticed. These are important considerations for the United States because even if classical scrapie is eliminated from the U.S. flock, atypical scrapie may continue to occur in a subset of the sheep population.

SHEEP HEALTH ISSUES 153 THREAT OF EMERGING OR EXISTING DISEASES Threat from an Existing Disease In the past decade, over 70 percent of the emerging diseases have been zoonotic (Woolhouse and Gowtage-Sequeria, 2005). The U.S. sheep indus- try has been fortunate to avoid a significant crisis resulting from a 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 such disease that should be reviewed is Johne’s disease. Johne’s disease is caused by Mycobacterium avium subspecies paratu- berculosis (MAP), which is a small bacterium related to Mycobacterium avium (avian TB). The organism affects cattle, sheep, and goats by causing a chronic inflammation of the intestines. The inflammation progresses to a severe state affecting the absorption of nutrients, which causes the animal to lose condition and eventually progress to death. Crohn’s disease is a hu- man condition that is also characterized by a chronic inflammation of the intestines. There is continuing research and debate as to whether the Johne’s agent is the causative agent or contributing factor for Crohn’s (Radostits et al., 2007) To date, there has been no definitive causal link between the two diseases. If a definitive link between Johne’s disease and Crohn’s disease, a chronic debilitating human disease, were made in the future, lamb meat and sheep milk and sheep milk products may come under scrutiny. The MAP organism has a waxy cell wall, tends to clump, and appears to be quite resistant to inactivation. Studies have shown the bacterium to survive pasteurization temperatures (Millar et al., 1996; Grant et al., 2002). The agent is shed in large amounts in the feces. Hence, contaminated feed, bedding, water, and soiled udders serve as sources of infection. Animals less than 6 months of age are thought to be most susceptible to infection. The incubation period for OJD is long, during which time the animal can be shedding the agent and be a source of infection for other sheep. Available diagnostic tests suffer from a number of problems. Infection is often dif- ficult to confirm during the incubation period. OJD may be confused with parasitism, chronic malnutrition, caseous lymphadenitis, and OPP. Control of the disease in infected flocks is currently difficult because there is no reli- able live animal test that can detect animals shedding very low numbers of MAP (Radostits et al., 2007). Ovine Johne’s disease has been documented on all continents. In the United States, OJD is estimated to be present on 4.7 percent of sheep opera- tions (USDA, 2004). Currently there is no national, state, or producer‑driven control program for OJD. For Johne’s disease in cattle, there is a voluntary program conducted by states with federal support. In the United States,

154 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES surveys have indicated that the primary problem is in the dairy cattle sector but it is also increasing in the nation’s beef cattle herd. If there were ever a definitive link made between Johne’s and Crohn’s or if the public perceived there was a risk, a number of food safety questions would need to be answered: • Given that the Johne’s agent is shed in large numbers (millions of organisms) in the feces, will fecal contamination of the carcass result in meat contaminated by this agent? If so, will the current microbial intervention steps be effective for this agent? • There is evidence that the Johne’s organism is present in lymph nodes. It would be difficult to process meat totally free of lymph nodes. Would this also provide a source of the organism in food for humans? • Can the agent survive cooking? • If the organism survives cooking, what interventions would be neces- sary to state that lamb and mutton are safe in the event a definitive link is made? • Given that studies have shown that the organism survives pasteuriza- tion, can sheep shed the agent in milk? Would sheep milk and sheep milk products be a risk? The National Advisory Committee on Microbial Criteria for Foods (USDA) has assigned a subcommittee to conduct an assessment of the food safety importance of MAP (USDA, 2006). The committee has been asked to limit its deliberations to the consideration of a very specific set of ques- tions. It has not been asked to consider the question of whether or not MAP is a human pathogen. The committee was asked to consider the following questions: • What food, water, or environmental sources are of most concern with respect to exposure of humans to MAP? • What are the frequencies and levels of MAP contamination found in the above-referenced sources? • What is the efficacy of the current methods of detection for MAP? • What processing interventions are available for the foods of concern to eliminate or reduce the levels of MAP contamination to an acceptable level or to ensure that MAP does not enter the food supply? • What are the research needs to determine additional sources of MAP; the frequencies and levels of MAP contamination in specific sources of concern; potential processing interventions to eliminate or reduce the levels of MAP contamination; and potential processing interventions to prevent MAP from entering the food supply?

SHEEP HEALTH ISSUES 155 Threat from a Foreign Animal Disease The findings of the NAHMS 2001 sheep study (USDA, 2003a) indicate that certain behaviors and lack of certain practices increase the vulnerability of many sheep operations to disease. One of the biggest vulnerabilities is the risk of introducing a foreign animal disease. When introduced into a native population, foreign animal diseases may spread rapidly as the animals have no immunity to the disease. In many cases, the outbreaks result in a high death loss and/or severe production losses. Foot‑and‑mouth disease is an example of such a disease. It is a highly contagious disease that affects cloven-hoofed animals, including pigs, cattle, sheep, and goats. The virus that causes the disease can spread rapidly over large distances, mainly from animal-to-animal contact or from contact with other contaminated sources. While the United States is currently free from this disease, the risk of introduction is real. The introduction could be ac- cidental through the illegal movement of animals or animal products, or intentional. The disease would have devastating consequences for the animal and allied industries. Initial outbreaks in an FMD-free country may warrant a full livestock movement stop for at least 1 week. A full movement stop of livestock prohibits the movement of all susceptible species (cattle, sheep, goats, swine, and other cloven-hoof species) from moving for any purpose including slaughter. Given the susceptibility of a broad range of species, the impact would affect not only the farm level, but also marketing and slaughtering channels, as well as meat and milk distribution. As an example, economic losses from the 2001 FMD epidemic in the United Kingdom ex- ceeded $10 billion (Thompson et al., 2002). More than 6 million animals were slaughtered. The outbreak lasted 7 months. A more recent outbreak that occurred in August 2007 was not widespread and was contained in a relatively short period of time, yet is still expected to result in millions of dollars of loss. In sheep, FMD results in signs that are often so subtle that they go un- noticed or the signs are mistaken for common sheep diseases, namely sore- mouth and foot rot. This is an important aspect of the disease, as infected sheep may be moved to many different locations and serve as a source of virus not only to other sheep and goats, but also spread the disease to pigs and cattle. In the 2001 UK outbreak, sheep were thought to play a major role in the widespread undetected initial spread of the disease. Other foreign animal diseases of concern are peste despetits ruminants, sheep and goat pox, exotic strains of bluetongue, and Rift Valley Fever. The threat of these diseases further emphasizes the need for a good biosecurity program as well as identification and records for traceability.

156 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES MAJOR ACCOMPLISHMENTS, OPPORTUNITIES, AND CHALLENGES IN SHEEP HEALTH Disease adversely impacts viability, overall growth, rate of gain, im- munity, and reproductive performance, which in turn reduce income. Flock health programs should be an essential component of the overall manage- ment scheme of raising sheep. Other than scrapie, there is no other disease where a national effort has been made to reduce or eliminate the problem. In the United States, making and prioritizing recommendations regarding research needs and control measures is difficult because the data related to the costs of disease and the effect on productivity and profitability of the sheep industry are inadequate. Major Accomplishments in Sheep Health The sheep industry and the USDA, with support from congressional appropriations, have made substantial progress in the effort to eradicate scrapie. The insidious nature of this disease in combination with the lack of definitive scientific understanding has made this a great challenge. A few of the more important accomplishments in sheep health include the following: • A reduced percentage of sheep of all face colors that test positive for scrapie at slaughter and a decrease in the number of positive animals found at slaughter, resulting in fewer new infected and source flocks and fewer animals indemnified in recent years. • A more complete animal identification system for sheep than exists for any other species in the United States, providing records of movements and a framework that would allow for the tracing of other diseases and animal movements. • The sheep industry was instrumental in obtaining designation of sheep within the MUMS Act, which has maintained the availability of criti- cally needed drugs, anthelmintics, and vaccines. Major Opportunities and Challenges for Sheep Health Over the years, the U.S. sheep industry has not suffered the effects of a major disease outbreak or a food safety crisis. Consequently, consumers do not currently associate lamb and mutton with Salmonella, E. coli, or other food-borne pathogens. From an animal welfare aspect, the practice of rais- ing sheep extensively has protected the industry from the severe criticism of those industries accused of having factory farms. The markets for lamb and other sheep products, such as milk, cheese, mutton, and wool, have the op-

SHEEP HEALTH ISSUES 157 portunity for growth unhampered by factors that may negatively influence public opinion and purchases. Other opportunities include: • Use of the identification system for animal movement as the founda- tion for an overall flock health program. The scrapie‑certification program could be used as the framework for other disease control programs. This is being done in Minnesota with OPP. • Improvement in biosecurity practices. Over time, the vast majority of sheep operations add sheep to their flocks (i.e., they do not maintain closed flocks). Despite these additions, most producers do not implement any type of quarantine, require premovement testing, or take precautions to prevent nose-to-nose contact at shows, or other encounters. The industry has the opportunity to improve biosecurity practices that will help reduce the spread of endemic diseases and prevent the entry of highly contagious diseases. • Genomics, gene biotechnology, gene markers. Although in its infancy in production applications, completion of mapping the sheep genome is like- ly to have major impacts on improving animal health and disease control. For example, New Zealand research has identified multiple gene markers for internal parasite resistance in sheep. New techniques are being used to provide improved medicines and vaccines. Despite the accomplishments and opportunities, a number of key chal- lenges in the area of sheep health still face the U.S. sheep industry, including the following: • Lack of data on the economic impacts or the true prevalence of most of the diseases or disease conditions affecting sheep in the United States. The lack of this information makes it difficult for the industry as a whole to make decisions regarding the allocation of resources as well as the determination of research and policy priorities. Without knowing the economic impacts and prevalence of certain diseases, individual producers may not be able to maximize profits by implementing the necessary on-farm preventive or control measures. • Lack of approved drugs. The unavailability of approved drugs will continue to adversely impact the sheep industry in efforts to prevent and control certain diseases. There will still be significant challenges of providing the necessary incentives for pharmaceutical companies to engage in research and development for small ruminant products. One of the biggest challenges will be the increasing drug resistance of intestinal parasites. • Growing shortage of large-animal veterinarians. The veterinarian shortage may add to the already significant number of sheep operations that do not use the service of a veterinarian, which, in turn, may affect sheep welfare. As the niche industries grow, many of the new sheep owners

158 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES 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 prog- ress the industry and USDA have made in reducing the prevalence of clas- sical 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 scien- tific 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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160 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES 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 Nor- wegian 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. Epi-���������� demiological and genetical differences between classical and atypical scrapie cases. Vet. Res. 38:65–80.

SHEEP HEALTH ISSUES 161 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 pasteur- ized 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. Polymor- phisms at codons 141 and 154 in the ovine prion protein gene are associated with scrapie Nor98 cases. J. Gen. Virol. 86:231−235. NAIS (National Animal Identification System). 2006. Sheep Working Group Report, August. Online at: http://www.sheepusa.org/?page=site/text&nav_id=bbe4ac2bced3271a5a8900 2b58b479de. 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.

162 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES 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 manage- ment 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 Reg- ister, 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 Myco- bacterium 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/ani- mal_diseases/scrapie/downloads/yearly_report_2006.pps. Accessed September 20, 2007.

SHEEP HEALTH ISSUES 163 USDA. 2007b. Scrapie Program September Monthly Report, FY 2007, Veterinary Ser- vices, 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.

164 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES 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. Sec- retary 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 ani- mals 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 emer- gency 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 quaran- tined 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 sur- veillance. 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.

SHEEP HEALTH ISSUES 165 1975 – Bloodline option was eliminated. Exposed animals could no longer be slaughtered for human consump- tion 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 commenta- tors 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.

166 CHANGES IN THE SHEEP INDUSTRY IN THE UNITED STATES 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. A voluntary scrapie flock certification program; b. One-time indemnification for infected and source flocks; and c. 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 Scra- pie 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.

SHEEP HEALTH ISSUES 167 Federal regulations that enacted the NSEP went into effect: (1) Records and identification required for sheep moving in interstate commerce, (2) in- demnity 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 com- munication, 2007).

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The U.S. sheep industry is complex, multifaceted, and rooted in history and tradition. The dominant feature of sheep production in the United States, and, thus, the focus of much producer and policy concern, has been the steady decline in sheep and lamb inventories since the mid-1940s. Although often described as "an industry in decline," this report concludes that a better description of the current U.S. sheep industry is "an industry in transition."

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