Veterinary Services Centers for Epidemiology and Animal Health July 2014 ______

Toxoplasma on U.S. Sheep

Operations

Background

Toxoplasma gondii is a protozoan parasite capable Esquivel C, et al., 2012); 61.0 percent of ewes in of infecting most warm-blooded animals, including 198 flocks in New Zealand (Dempster RP, et al., humans. It is estimated that 60 million people in the 2011); and 74.0 percent of sheep in 227 flocks in United States are infected with T. gondii, although Great Britain (Hutchinson JP, 2011). In the United few demonstrate symptoms because their immune States, 27.1 percent of slaughter lambs originating system prevents clinical disease. The Centers for from flocks in Maryland, Virginia, and West Virginia Disease Control considers toxoplasma to be a were positive for T. gondii (Dubey et al., 2008). leading cause of death attributed to foodborne 1 illness in the United States. Toxoplasma can be Sheep 2011 study transmitted to people through ingestion of contaminated meat (especially pork and lamb), In 2011, the USDA’s National Animal Health water, or contact with cat feces contaminated with Monitoring System conducted a study of U.S. T. gondii oocysts. Cats are the natural reservoir for sheep operations. The Sheep 2011 study was T. gondii and can shed millions of oocysts in their conducted in 22 of the Nation’s major sheep- feces for up to 3 weeks after infection. producing States,2 which were divided into 3 Toxoplasma is a concern to the sheep industry regions. Operations with more than one ewe met because it is an important cause of reproductive the study inclusion criteria. These operations losses in sheep, resulting in significant economic collectively represented 85.5 percent of the U.S. impacts. Susceptible sheep become infected with ewe inventory and 70.1 percent of U.S. farms with T. gondii by ingesting the oocysts excreted in cat ewes. feces. These oocysts can be found in contaminated feed, bedding, pasture, and water and remain Sheep 2011 Participating States infectious for long periods. Newly infected pregnant WA

MT ME ID ewes may abort or reabsorb their fetuses or may ND MN deliver stillborn, mummified, or weak lambs. Ewes OR WI SD VT NH WY MI infected prior to pregnancy develop an immune MA CA NY CT NV RI IA UT NE PA response that helps protect against clinical disease IL OH IN NJ CO MD DE during a subsequent pregnancy. MO KS WV VA

Flocks can experience a variety of lambing AZ KY NM NC OK outcomes due to T. gondii. In a Texas flock of TX AR TN SC GA 39 ewes experiencing an abortion storm in 2005, MS AL LA 14 healthy lambs were born, while 53 lambs or Regions FL fetuses (79.1 percent of lamb crop) were aborted, West Central resorbed, mummified, or stillborn. T. gondii East antibodies were detected in 94.8 percent of these ewes (Edwards and Dubey, 2013). The seroprevalence of T. gondii varies greatly in world sheep populations, e.g., 15.5 percent of sheep in Mexico’s Durango State (Alvarado- 2 California, Colorado, Idaho, Iowa, Kansas, Kentucky, Michigan, Minnesota, Missouri, Montana, New Mexico, New York, Ohio, Oregon, Pennsylvania, South Dakota, Texas, Utah, 1 CDC-http://www.cdc.gov/parasites/toxoplasmosis Virginia, Washington, Wisconsin, and Wyoming.

United States Department of Agriculture • Animal and Plant Health Inspection Service • Safeguarding American Agriculture The Sheep 2011 study focused on sheep health There was no substantial difference in the and management and was the first study to percentage of operations seropositive by estimate the national seroprevalence of management type (fig. 2) or by flock size (fig. 3). toxoplasmosis in U.S. lambs. Interestingly, when For flocks with at least one seropositive animal, the asked about familiarity with toxoplasmosis, average within flock prevalence was 54.0 percent of producers had never heard of the 28.9 percent (data not shown). disease or knew of it by name only. During the study, data and samples relevant to Figure 2. Percentage of operations and percentage the causes of abortion storms in sheep were of sheep seropositive for toxoplasma, by collected. In total, blood samples from 3,967 lambs management type from 353 participating operations were tested for Percent T. gondii antibodies at the Beltsville Agriculture Research Service using the modified agglutination 60 Operations test. T. gondii antibody seroprevalence indicates an 52.3 animal has been previously exposed to T. gondii. Sheep Estimates were weighted within size strata and 43.2 State, adjusting for nonresponse. 41.9 40 Toxoplasma prevalence in U.S. lambs 35.0

Flock-level prevalence

6.7 At least one lamb was seropositive for T. gondii 20 on 47.3 percent of operations. A higher percentage 11.2 of operations in the East region (58.8 percent) than 9.4 the Central region (34.6 percent) had lambs 13.6 seropositive for T. gondii (fig. 1). 4.0 0 Open Fenced Pasture Dry lot Figure 1. Percentage of operations and percentage range range of lambs seropositive for toxoplasma, by region Management type

Percent 80

Operations Lambs 60 58.8

47.3 40.0 75.7 40 34.6

20 17.1

9.8 9.5 5.5

0 West CentralEast All Region

United States Department of Agriculture • Animal and Plant Health Inspection Service • Safeguarding American Agriculture Figure 3. Percentage of operations and percentage of Presence of cats lambs seropositive for toxoplasma, by flock size Cats are a known risk for T. gondii transmission Percent to sheep. Newly infected cats typically excrete large 60 Operations numbers of oocysts in their feces and can 54.5 Lambs contaminate bedding, unprotected hay, feed bins, water, and pastures. Nearly all operations 3 45.4 (96.2 percent) had some type of cat present during 2010. The majority of operations had domestic cats 40 39.1 with outside access (80.1 percent) or feral/stray cats (77.9 percent). Rodents persistently infected with T. gondii are an important source of infection for cats that hunt them. Birds can also be a source of infection for cats. 20 14.5 Conclusions 12.8 Nearly half of U.S. sheep operations were 5.5 seropositive for T. gondii, confirming recent or past exposure to this parasitic infection. Flock 0 Large Medium Small management, size, and geographic location appear (20-99) (100-499) (500 or more) to impact the percentage of operations and lambs Flock size (number of ewes) seropositive for toxoplasma antibodies.

Sheep operations can reduce the likelihood that Animal-level prevalence their animals will become infected with T. gondii by following good biosecurity practices and by Overall, 9.4 percent of lambs tested positive for eliminating known risk factors. Such practices might T. gondii antibodies. Similar to flock-level results, a include preventing cats from accessing sheep and higher percentage of lambs in the East region than feed storage areas and reducing rodent the Central region were seropositive (17.1 and populations. Previously infected mature cats are 5.5 percent, respectively). Although there was no less likely to shed Toxoplasma. substantial difference between management types To reduce the risk of human infection, lamb at the operation level, a higher percentage of lambs should be thoroughly cooked before eating, and managed primarily on pasture were seropositive for good hygiene should be practiced when changing T. gondii compared with lambs managed primarily cat litter boxes or working with potentially on open or fenced range (figure 2). A higher contaminated soil. percentage of lambs on small operations than large operations tested seropositive (14.5 and References 5.4 percent, respectively) [fig. 3]. Alvarado-Esquivel C, et al., 2012. Seroprevalence Abortions on U.S. Sheep operations of Toxoplasma gondii infection in domestic sheep in Durango State, Mexico. J Parasitol 98(2); 271–273.

Of operations with more than one ewe, nearly Alvarado-Esquivel C, et al., 2013. Seroprevalence half (43.8 percent) had ewes that aborted in 2010. and correlates of Toxoplasma gondii infection in Nearly three-fourths of these operations domestic sheep in Michnoacan State, Mexico. Prev (73.8 percent) indicated that the cause of abortion Vet Med 112(3-4); 433–437. was unknown. Just 3.4 percent of operations indicated the suspected cause of abortions was Behymer DE, et al., 1985. Epidemiologic study of due to toxoplasmosis. A low percentage of these toxoplasmosis on a sheep ranch. Am J Vet Res operations (6.9 percent) indicated that the 46(5); 1141–1144. diagnosis was confirmed by a veterinarian or laboratory.

3 Outdoor domestic or indoor with outside access; feral or stray; or wild or exotic).

United States Department of Agriculture • Animal and Plant Health Inspection Service • Safeguarding American Agriculture Dempster RP, et al., 2011. Serological survey of ______Toxoplasma gondii and Campylobacter fetus in sheep from New Zealand. New Zeal Vet J For more information, contact: USDA–APHIS–VS–CEAH–NAHMS 59(4); 155–159. NRRC Building B, M.S. 2E7 2150 Centre Avenue Dubey JP, et al., 2008. High prevalence and Fort Collins, CO 80526-8117 abundant atypical genotypes of Toxoplasma gondii 970.494.7000 http://www.aphis.usda.gov/nahms isolated from lambs destined for human #694.0514 consumption in the USA. Intl J Parasitol 38(8–9); 999–1006. The U.S. Department of Agriculture (USDA) prohibits discrimination in all its programs and activities on the basis of Dubey JP, 2010. Toxoplasmosis of Animals and race, color, national origin, age, disability, and where nd applicable, sex, marital status, familial status, parental status, Humans, 2 ed. CRC Press, Taylor & Francis religion, sexual orientation, genetic information, political beliefs, Group, Boca Raton, FL. reprisal, or because all or part of an individual’s income is derived from any public assistance program. (Not all Edwards JF, Dubey JP, 2013. Toxoplasma gondii prohibited bases apply to all programs.) Persons with disabilities who require alternative means for communication of abortion storm in sheep on a Texas farm and program information (Braille, large print, audiotape, etc.) isolation of mouse virulent atypical genotype T. should contact USDA’s TARGET Center at (202) 720–2600 gondii from an aborted lamb from a chronically (voice and TDD). To file a complaint of discrimination, write to infected ewe. Vet Parasitol 192(1–3); 129–136. USDA, Director, Office of Civil Rights, 1400 Independence Avenue, S.W., Washington, D.C. 20250–9410, or call (800) 795–3272 (voice) or (202) 720–6382 (TDD). USDA is an equal Hutchinson JP, 2011. Survey to determine the opportunity provider and employer. seroprevalence of Toxoplasma gondii infection in British sheep flocks. Vet Rec 169; 582. Mention of companies or commercial products does not imply recommendation or endorsement by the U.S. Department of Agriculture over others not mentioned. USDA neither Tumurjav B, et al., 2010. Serodiagnosis of ovine guarantees nor warrants the standard of any product toxoplasmosis in Mongolia by an enzyme linked mentioned. Product names are mentioned solely to report immunosorbent assay with recombinnt Toxoplasma factually on available data and to provide specific information. gondii matrix antigen 1. Jap J Vet Res 58(2); 111– 119.

United States Department of Agriculture • Animal and Plant Health Inspection Service • Safeguarding American Agriculture