{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,31]],"date-time":"2026-10-31T06:33:22Z","timestamp":1793428402815,"version":"4.5.0"},"reference-count":51,"publisher":"Wildlife Disease Association","issue":"1","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Journal of Wildlife Diseases"],"published-print":{"date-parts":[[2023,4,25]]},"abstract":"<jats:p>Low lamb recruitment can be an obstacle to bighorn sheep (Ovis canadensis) conservation and restoration. Causes of abortion and neonate loss in bighorn sheep, which may affect recruitment, are poorly understood. Toxoplasma gondii is a major cause of abortion and stillbirth in domestic small ruminants worldwide, but no reports exist documenting abortion or neonatal death in bighorn sheep attributable to toxoplasmosis. Between March 2019 and May 2021, eight fetal and neonatal bighorn lamb cadavers from four western US states (Idaho, Montana, Nebraska, and Washington) were submitted to the Washington Animal Disease Diagnostic Laboratory for postmortem examination, histologic examination, and ancillary testing to determine the cause of abortion or neonatal death. Necrotizing encephalitis characteristic of toxoplasmosis was identified histologically in six of eight cases, and T. gondii infection was confirmed by PCR in five cases with characteristic lesions. Other lesions attributable to toxoplasmosis were pneumonia (3\/5 cases) and myocarditis (2\/5 cases). Protozoal cysts were identified histologically within brain, lung, heart, skeletal muscle, adipose tissue, or a combination of samples in all five sheep with PCR-confirmed T. gondii infections. Seroprevalence of T. gondii ranged from 40\u201381% of adult females sampled in the Washington population in October and November 2018\u20132021, confirming high rates of exposure before detection of Toxoplasma abortions in this study. Of 1,149 bighorn sheep postmortem samples submitted to Washington Animal Disease Diagnostic Laboratory between January 2000 and May 2021, 21 of which were from fetuses or neonates, a single case of chronic toxoplasmosis was diagnosed in one adult ewe. Recent identification of Toxoplasma abortions in bighorn sheep suggests that toxoplasmosis is an underappreciated cause of reproductive loss. Abortions and neonatal mortalities should be investigated through postmortem and histologic examination, particularly in herds that are chronically small, demographically stagnant, or exhibit reproductive rates lower than expected.<\/jats:p>","DOI":"10.7589\/jwd-d-22-00057","type":"journal-article","created":{"date-parts":[[2023,4,25]],"date-time":"2023-04-25T00:49:45Z","timestamp":1682383785000},"page":"37-48","source":"Crossref","is-referenced-by-count":4,"title":["ABORTION AND NEONATAL MORTALITY DUE TO TOXOPLASMA GONDII IN BIGHORN SHEEP (OVIS CANADENSIS)"],"prefix":"10.7589","volume":"59","author":[{"given":"Elis A.","family":"Fisk","sequence":"first","affiliation":[{"name":"Washington Animal Disease Diagnostic Laboratory, 1940 SE Olympia Ave., Pullman, Washington 99164-7034, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"E. Frances","family":"Cassirer","sequence":"additional","affiliation":[{"name":"Idaho Department of Fish and Game, 3316 16th St., Lewiston, Idaho 83501, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Katey S.","family":"Huggler","sequence":"additional","affiliation":[{"name":"Department of Fish and Wildlife Sciences, University of Idaho, 875 Perimeter Dr., Moscow, Idaho 83844, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Allan P.","family":"Pessier","sequence":"additional","affiliation":[{"name":"Washington Animal Disease Diagnostic Laboratory, 1940 SE Olympia Ave., Pullman, Washington 99164-7034, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura A.","family":"White","sequence":"additional","affiliation":[{"name":"Washington Animal Disease Diagnostic Laboratory, 1940 SE Olympia Ave., Pullman, Washington 99164-7034, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joshua D.","family":"Ramsay","sequence":"additional","affiliation":[{"name":"Washington Animal Disease Diagnostic Laboratory, 1940 SE Olympia Ave., Pullman, Washington 99164-7034, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth W.","family":"Goldsmith","sequence":"additional","affiliation":[{"name":"Washington Animal Disease Diagnostic Laboratory, 1940 SE Olympia Ave., Pullman, Washington 99164-7034, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Holly R.","family":"Drankhan","sequence":"additional","affiliation":[{"name":"Washington Animal Disease Diagnostic Laboratory, 1940 SE Olympia Ave., Pullman, Washington 99164-7034, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rebecca M.","family":"Wolking","sequence":"additional","affiliation":[{"name":"Washington Animal Disease Diagnostic Laboratory, 1940 SE Olympia Ave., Pullman, Washington 99164-7034, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kezia R.","family":"Manlove","sequence":"additional","affiliation":[{"name":"Department of Wildland Resources and Ecology Center, Utah State University, 5230 Old Main Hill, NR 206, Logan, Utah 84322, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Todd","family":"Nordeen","sequence":"additional","affiliation":[{"name":"Nebraska Game and Parks Commission, 2200 N 33rd St., PO Box 30370, Lincoln, Nebraska 68503, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John T.","family":"Hogg","sequence":"additional","affiliation":[{"name":"Montana Conservation Science Institute Ltd., 5200 Miller Creek Rd., Missoula, Montana 59803, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kyle R.","family":"Taylor","sequence":"additional","affiliation":[{"name":"Washington Animal Disease Diagnostic Laboratory, 1940 SE Olympia Ave., Pullman, Washington 99164-7034, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4415","reference":[{"key":"24","doi-asserted-by":"crossref","unstructured":"K Hatam-Nahavandi, R Calero-Bernal, MT Rahimi, et al.  \"Sci Rep.\"  11, \"Toxoplasma gondii infection in domestic and wild felids as public health concerns: a systematic review and meta-analysis.\" 9509 (2021)","DOI":"10.1038\/s41598-021-89031-8"},{"key":"23","doi-asserted-by":"crossref","unstructured":"JL Grigg, LL Wolfe, KA Fox, et al.  \"J Wildl Dis.\"  53, \"Assessing timing and causes of neonatal lamb losses in a bighorn sheep (Ovis canadensis canadensis) herd via use of vaginal implant transmitters.\" 596 (2017)","DOI":"10.7589\/2016-10-239"},{"key":"25","doi-asserted-by":"crossref","unstructured":"WL Homan, M Vercammen, J De Braekeleer, et al.  \"Int J Parasitol.\"  30, \"Identification of a 200- to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR.\" 69 (2000)","DOI":"10.1016\/S0020-7519(99)00170-8"},{"key":"4","doi-asserted-by":"crossref","unstructured":"SN Bevins, S Carver, EE Boydston, et al.  \"PLoS One.\"  7, \"Three pathogens in sympatric populations of pumas, bobcats, and domestic cats: Implications for infectious disease transmission.\" e31403 (2012)","DOI":"10.1371\/journal.pone.0031403"},{"key":"36","doi-asserted-by":"crossref","unstructured":"J Paul-Murphy, T Work, D Hunter, et al.  \"J Wildl Dis.\"  30, \"Serologic survey and serum biochemical reference ranges of the free-ranging mountain lion (Felis concolor) in California.\" 205 (1994)","DOI":"10.7589\/0090-3558-30.2.205"},{"key":"31","doi-asserted-by":"crossref","unstructured":"MA Miller, WA Miller, PA Conrad, et al.  \"Int J Parasitol.\"  38, \"Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: New linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters.\" 1319 (2008)","DOI":"10.1016\/j.ijpara.2008.02.005"},{"key":"49","doi-asserted-by":"crossref","unstructured":"E Vanwormer, PA Conrad, MA Miller, et al.  \"EcoHealth.\"  10, \"Toxoplasma gondii, source to sea: Higher contribution of domestic felids to terrestrial parasite loading despite lower infection prevalence.\" 277 (2013)","DOI":"10.1007\/s10393-013-0859-x"},{"key":"26","doi-asserted-by":"crossref","unstructured":"B Jacob, BM Debey, D Bradway,  \"Vet Pathol.\"  43, \"Spinal intradural Mycobacterium haemophilum granuloma in an American bison (Bison bison).\" 998 (2006)","DOI":"10.1354\/vp.43-6-998"},{"key":"35","doi-asserted-by":"crossref","unstructured":"P Olias, AD Gruber, AO Heydorn, et al.  \"Avian Pathol.\"  38, \"A novel Sarcocystisassociated encephalitis and myositis in racing pigeons.\" 121 (2009)","DOI":"10.1080\/03079450902737847"},{"key":"33","unstructured":"\"Basic local alignment search tool (BLAST).\"  (2022)"},{"key":"1","unstructured":"AO Aganga, JU Umoh, EK Kyewalabye, et al.  \"J Anim Prod Res.\"  8, \"Comparative experimental transmission studies with Nigerian isolates and TS 1 strain of Toxoplasma gondii in sheep.\" 104 (1988)"},{"key":"2","doi-asserted-by":"crossref","unstructured":"TV Baszler, JP Dubey, CV L\u00f6hr, et al.  \"J Wildl Dis.\"  36, \"Toxoplasmic encephalitis in a free-ranging rocky mountain bighorn sheep from Washington.\" 752 (2000)","DOI":"10.7589\/0090-3558-36.4.752"},{"key":"3","doi-asserted-by":"crossref","unstructured":"TE Besser, EF Cassirer, A Lisk, et al.  \"Ecol Evol.\"  11, \"Natural history of a bighorn sheep pneumonia epizootic: Source of infection, course of disease, and pathogen clearance.\" 14366 (2021)","DOI":"10.1002\/ece3.8166"},{"key":"5","doi-asserted-by":"crossref","unstructured":"A Brower, KM Homb, P Bochsler, et al.  \"J Vet Diagn Inves.\"  20, \"Encephalitis in aborted bovine fetuses associated with bovine herpesvirus 1 infection.\" 297 (2008)","DOI":"10.1177\/104063870802000306"},{"key":"6","doi-asserted-by":"crossref","unstructured":"D Buxton, DA Blewett, AJ Trees, et al.  \"J Comp Pathol.\"  98, \"Further studies in the use of monensin in the control of experimental ovine toxoplasmosis.\" 225 (1988)","DOI":"10.1016\/0021-9975(88)90021-7"},{"key":"7","doi-asserted-by":"crossref","unstructured":"D Buxton, JS Gilmour, KW Angus, et al.  \"Res Vet Sci.\"  32, \"Perinatal changes in lambs infected with Toxoplasma gondii.\" 170 (1982)","DOI":"10.1016\/S0034-5288(18)32408-1"},{"key":"8","doi-asserted-by":"crossref","unstructured":"D Buxton, K Thomson, S Maley, et al.  \"Vet Rec.\"  129, \"Vaccination of sheep with a live incomplete strain (S48) of Toxoplasma gondii and their immunity to challenge when pregnant.\" 89 (1991)","DOI":"10.1136\/vr.129.5.89"},{"key":"9","doi-asserted-by":"crossref","unstructured":"JW Cain, RC Karsch, EJ Goldstein, et al.  \"J Wildl Manage.\"  83, \"Survival and cause-specific mortality of desert bighorn sheep lambs.\" 251 (2019)","DOI":"10.1002\/jwmg.21597"},{"key":"10","doi-asserted-by":"crossref","unstructured":"EF Cassirer  and ARE Sinclair  \"J Wildl Manage.\"  71, \"Dynamics of pneumonia in a bighorn sheep metapopulation.\" 1080 (2007)","DOI":"10.2193\/2006-002"},{"key":"11","doi-asserted-by":"crossref","unstructured":"E Collantes-Fern\u00e1ndez, A Zaballos, G Alvarez-Garc\u00eda, et al.  \"J Clin Microbiol.\"  40, \"Quantitative detection of Neospora caninum in bovine aborted fetuses and experimentally infected mice by real-time PCR.\" 1194 (2002)","DOI":"10.1128\/JCM.40.4.1194-1198.2002"},{"key":"12","doi-asserted-by":"crossref","unstructured":"JL Davies, GJ Haldorson, DS Bradway, et al.  \"J Vet Diagn Invest.\"  23, \"Fatal hepatic sarcocystosis in a captive black bear (Ursus americanus) associated with Sarcocystis canis\u2013like infection.\" 379 (2011)","DOI":"10.1177\/104063871102300234"},{"key":"13","doi-asserted-by":"crossref","unstructured":"JP. Dubey,  \"Vet Parasitol.\"  163, \"Toxoplasmosis in sheep\u2014The last 20 years.\" 1 (2009)","DOI":"10.1016\/j.vetpar.2009.02.026"},{"key":"14","doi-asserted-by":"crossref","unstructured":"JP. Dubey,  \"Toxoplasmosis of animals and humans.\"  \"Techniques for studying Toxoplasma gondii.\" 91 (2022a)","DOI":"10.1201\/9781003199373-3"},{"key":"15","doi-asserted-by":"crossref","unstructured":"JP. Dubey,  \"Toxoplasmosis of animals and humans.\"  \"Toxoplasma gondii infections in sheep.\" 217 (2022b)","DOI":"10.1201\/9781003199373-8"},{"key":"16","doi-asserted-by":"crossref","unstructured":"JP Dubey  and WJ Foreyt  \"J Parasitol.\"  86, \"Seroprevalence of Toxoplasma gondii in Rocky Mountain bighorn sheep (Ovis canadensis).\" 622 (2000)","DOI":"10.2307\/3284883"},{"key":"17","doi-asserted-by":"crossref","unstructured":"JP Dubey  and CA Kirkbride  \"J Am Vet Med Assoc.\"  195, \"Economic and public health considerations of congenital toxoplasmosis in lambs.\" 1715 (1989)","DOI":"10.2460\/javma.1989.195.12.1715"},{"key":"18","doi-asserted-by":"crossref","unstructured":"JP Dubey  and DS Lindsay  \"Vet Clin North Am Food Anim Pract.\"  22, \"Neosporosis, toxoplasmosis, and sarcocystosis in ruminants.\" 645 (2006)","DOI":"10.1016\/j.cvfa.2006.08.001"},{"key":"19","doi-asserted-by":"crossref","unstructured":"JP Dubey, FHA Murata, CK Cerqueira-C\u00e9zar, et al.  \"Vet Parasitol.\"  286, \"Economic and public health importance of Toxoplasma gondii infections in sheep: 2009\u20132020.\" 109195 (2020)","DOI":"10.1016\/j.vetpar.2020.109195"},{"key":"20","unstructured":"HN. Elliot,  \"Desert Bighorn Counc Trans.\"  5, \"Bobcats and bighorn sheep.\" 38 (1961)"},{"key":"21","doi-asserted-by":"crossref","unstructured":"LF Elliott, WM Boyce, RK Clark, et al.  \"J Wildl Dis.\"  30, \"Geographic analysis of pathogen exposure in bighorn sheep (Ovis canadensis).\" 315 (1994)","DOI":"10.7589\/0090-3558-30.3.315"},{"key":"22","doi-asserted-by":"crossref","unstructured":"TJ Garwood, CP Lehman, DP Walsh, et al.  \"Ecol Evol.\"  10, \"Removal of chronic Mycoplasma ovipneumoniae carrier ewes eliminates pneumonia in a bighorn sheep population.\" 3491 (2020)","DOI":"10.1002\/ece3.6146"},{"key":"27","doi-asserted-by":"crossref","unstructured":"Y Kikuchi, BB Chomel, RW Kasten, et al.  \"Vet Parasitol.\"  120, \"Seroprevalence of Toxoplasma gondii in American free-ranging or captive pumas (Felis concolor) and bobcats (Lynx rufus).\" 1 (2004)","DOI":"10.1016\/j.vetpar.2004.01.002"},{"key":"28","doi-asserted-by":"crossref","unstructured":"DS Lindsay  and JP Dubey  \"Vet Clin North Am Food Anim Pract.\"  36, \"Neosporosis, toxoplasmosis, and sarcocystosis in ruminants: An update.\" 205 (2020)","DOI":"10.1016\/j.cvfa.2019.11.004"},{"key":"29","doi-asserted-by":"crossref","unstructured":"S. Martin,  \"Neonatal Netw.\"  20, \"Congenital toxoplasmosis.\" 23 (2001)","DOI":"10.1891\/0730-0832.20.4.23"},{"key":"30","doi-asserted-by":"crossref","unstructured":"J Menotti, YJF Garin, P Thulliez, et al.  \"Clin Microbiol Infect.\"  16, \"Evaluation of a new 5\u2032-nuclease real-time PCR assay targeting the Toxoplasma gondii AF146527 genomic repeat.\" 363 (2010)","DOI":"10.1111\/j.1469-0691.2009.02809.x"},{"key":"32","doi-asserted-by":"crossref","unstructured":"NB Mugridge, DA Morrison, AM Johnson, et al.  \"Int J Parasitol.\"  29, \"Phylogenetic relationships of the genus Frenkelia: A review of its history and new knowledge gained from comparison of large subunit ribosomal ribonucleic acid gene sequences.\" 957 (1999)","DOI":"10.1016\/S0020-7519(99)00062-4"},{"key":"34","doi-asserted-by":"crossref","unstructured":"T Nayeri, S Sarvi, M Moosazadeh, et al.  \"Vet Parasitol.\"  290, \"Global prevalence of Toxoplasma gondii infection in the aborted fetuses and ruminants that had an abortion: A systematic review and meta-analysis.\" 109370 (2021)","DOI":"10.1016\/j.vetpar.2021.109370"},{"key":"37","unstructured":"R. Puls,  \"Mineral levels in animal health: bibliographies.\"  356 (1994)"},{"key":"38","unstructured":"F Riaz, I Rashid, H Akbar, et al.  \"Iran J Parasitol.\"  11, \"DNA amplification techniques for the detection of Toxoplasma gondii tissue cysts in meat producing animals: A narrative review article.\" 431 (2016)"},{"key":"39","doi-asserted-by":"crossref","unstructured":"HP Riemann, JA Howarth, R Ruppanner, et al.  \"J Wildl Dis.\"  11, \"Toxoplasma antibodies among bobcats and other carnivores of northern California.\" 272 (1975)","DOI":"10.7589\/0090-3558-11.2.272"},{"key":"40","doi-asserted-by":"crossref","unstructured":"EM. Rominger,  \"J Wildl Manage.\"  82, \"The Gordian knot of mountain lion predation and bighorn sheep.\" 19 (2018)","DOI":"10.1002\/jwmg.21396"},{"key":"41","doi-asserted-by":"crossref","unstructured":"PI Ross, MG Jalkotzy, M Festa-Bianchet,  \"Can J Zool.\"  75, \"Cougar predation on bighorn sheep in southwestern Alberta.\" 771 (1997)","DOI":"10.1139\/z97-098"},{"key":"42","doi-asserted-by":"crossref","unstructured":"KJ Schwab  and JJ McDevitt  \"Appl Environ Microbiol.\"  69, \"Development of a PCR-enzyme immunoassay oligoprobe detection method for Toxoplasma gondii oocysts, incorporating PCR controls.\" 5819 (2003)","DOI":"10.1128\/AEM.69.10.5819-5825.2003"},{"key":"43","doi-asserted-by":"crossref","unstructured":"FJ Singer, E Williams, MW Miller, et al.  \"Restor Ecol.\"  8, \"Population growth, fecundity, and survivorship in recovering populations of bighorn sheep.\" 75 (2000)","DOI":"10.1046\/j.1526-100x.2000.80067.x"},{"key":"44","doi-asserted-by":"crossref","unstructured":"MA Sirochman, KJ Woodruff, JL Grigg, et al.  \"J Wildl Dis.\"  48, \"Evaluation of management treatments intended to increase lamb recruitment in a bighorn sheep herd.\" 781 (2012)","DOI":"10.7589\/0090-3558-48.3.781"},{"key":"45","doi-asserted-by":"crossref","unstructured":"JB Smith, JA Jenks, TW Grovenburg, et al.  \"PLoS One.\"  9, \"Disease and predation: Sorting out causes of a bighorn sheep (Ovis canadensis) decline.\" e88271 (2014a)","DOI":"10.1371\/journal.pone.0088271"},{"key":"46","doi-asserted-by":"crossref","unstructured":"JB Smith, DP Walsh, EJ Goldstein, et al.  \"Wildl Soc Bull.\"  38, \"Techniques for capturing bighorn sheep lambs.\" 165 (2014b)","DOI":"10.1002\/wsb.360"},{"key":"47","unstructured":"\"Comprehensive conservation plan, national bison range.\"  (2019)"},{"key":"48","doi-asserted-by":"crossref","unstructured":"W Van Dyke, A Sands, J Yoakum, et al.  \"Wildlife habitats in managed rangelands\u2014The Great Basin of southeastern Oregon. General Technical Report PNW-GTR-159.\"  36 (1983)","DOI":"10.2737\/PNW-GTR-159"},{"key":"50","unstructured":"\"Management plan for the 4-0 ranch unit of the Chief Joseph Wildlife Area.\"  (2019)"},{"key":"51","doi-asserted-by":"crossref","unstructured":"AG Wilson, S Wilson, N Alavi, et al.  \"Proc R Soc B Biol Sci.\"  288, \"Human density is associated with the increased prevalence of a generalist zoonotic parasite in mammalian wildlife.\" 20211724 (2021)","DOI":"10.1098\/rspb.2021.1724"}],"container-title":["Journal of Wildlife Diseases"],"original-title":[],"deposited":{"date-parts":[[2026,10,31]],"date-time":"2026-10-31T06:00:08Z","timestamp":1793426408000},"score":1,"resource":{"primary":{"URL":"https:\/\/bioone.org\/journals\/journal-of-wildlife-diseases\/volume-59\/issue-1\/JWD-D-22-00057\/ABORTION-AND-NEONATAL-MORTALITY-DUE-TO-TOXOPLASMA-GONDII-IN-BIGHORN\/10.7589\/JWD-D-22-00057.full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,25]]},"references-count":51,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,1,1]]}},"URL":"https:\/\/doi.org\/10.7589\/jwd-d-22-00057","relation":{},"ISSN":["0090-3558","1943-3700"],"issn-type":[{"value":"0090-3558","type":"print"},{"value":"1943-3700","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,25]]}}}