{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,16]],"date-time":"2026-07-16T16:55:49Z","timestamp":1784220949508,"version":"3.55.0"},"reference-count":40,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2022,10,3]],"date-time":"2022-10-03T00:00:00Z","timestamp":1664755200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Toxoplasma gondii is one of the most common protozoan parasites and is widely present in all warm-blooded animals. Although clinical disease is uncommon, some species, including ring-tailed lemurs (Lemur catta), have been found to develop acute and lethal toxoplasmosis. The aim of this study was to describe the pathologic, immunohistochemical, serological, and molecular findings of an outbreak of fatal toxoplasmosis in three captive ring-tailed lemurs in Central Italy in 2009. The animals died acutely within few days. The necropsy was immediately performed; necrotic lesions in the spleen, liver, and kidney, as well as interstitial pneumonia, were found histologically. All animals had high titers of anti\u2013T. gondii-specific antibodies (1:1280 IgM and 1:640 IgG) according to a modified agglutination test (MAT) and immunohistochemistry showed scattered tachyzoites in the target organs. Diagnosis was confirmed by PCR and clonal type II was identified. In addition, the seven co-habiting lemurs were seronegative. This paper reports the first outbreak of acute disseminated toxoplasmosis in captive ring-tailed lemurs in Italy. These findings confirm the high susceptibility of this endangered species to toxoplasma infection, which may be considered a further threat to captive population viability.<\/jats:p>","DOI":"10.3390\/pathogens11101142","type":"journal-article","created":{"date-parts":[[2022,10,10]],"date-time":"2022-10-10T01:21:07Z","timestamp":1665364867000},"page":"1142","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Toxoplasmosis in Captive Ring-Tailed Lemurs (Lemur catta)"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-3742-7636","authenticated-orcid":false,"given":"Guido","family":"Rocchigiani","sequence":"first","affiliation":[{"name":"Department of Veterinary Anatomy, Physiology and Pathology, Institute of Infection, Veterinary and Ecological Sciences, Leahurst Campus, University of Liverpool, Chester High Road, Neston CH64 7TE, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9102-5566","authenticated-orcid":false,"given":"Niccol\u00f2","family":"Fonti","sequence":"additional","affiliation":[{"name":"Dipartimento di Scienze Veterinarie, Universit\u00e0 di Pisa, Viale delle Piagge, 2-56124 Pisa, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9095-6326","authenticated-orcid":false,"given":"Simona","family":"Nardoni","sequence":"additional","affiliation":[{"name":"Dipartimento di Scienze Veterinarie, Universit\u00e0 di Pisa, Viale delle Piagge, 2-56124 Pisa, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paolo","family":"Cavicchio","sequence":"additional","affiliation":[{"name":"Giardino Zoologico di Pistoia, Via pieve a Celle 160a, 51100 Pistoia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3301-3778","authenticated-orcid":false,"given":"Francesca","family":"Mancianti","sequence":"additional","affiliation":[{"name":"Dipartimento di Scienze Veterinarie, Universit\u00e0 di Pisa, Viale delle Piagge, 2-56124 Pisa, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1254-5772","authenticated-orcid":false,"given":"Alessandro","family":"Poli","sequence":"additional","affiliation":[{"name":"Dipartimento di Scienze Veterinarie, Universit\u00e0 di Pisa, Viale delle Piagge, 2-56124 Pisa, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,10,3]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1863-2378.2009.01276.x","article-title":"A Brief History and Overview of Toxoplasma gondii","volume":"57","author":"Innes","year":"2010","journal-title":"Zoonoses Public Health"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1217","DOI":"10.1016\/S0020-7519(00)00124-7","article-title":"Toxoplasma gondii: From animals to humans","volume":"30","author":"Tenter","year":"2000","journal-title":"Int. J. Parasitol."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Dubey, J.P. (2022). Toxoplasmosis of Animals and Humans, CRC Press. [3rd ed.].","DOI":"10.1201\/9781003199373"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1007\/s11686-021-00507-z","article-title":"Toxoplasma gondii Infection in Marine Animal Species, as a Potential Source of Food Contamination: A Systematic Review and Meta-Analysis","volume":"67","author":"Ahmadpour","year":"2022","journal-title":"Acta Parasit."},{"key":"ref_5","unstructured":"Dubey, J.P. (2010). Toxoplasmosis of Animals and Humans, CRC Press. [2nd ed.]."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"100002","DOI":"10.1016\/j.eas.2022.100002","article-title":"Clinical toxoplasmosis in zoo animals and its management","volume":"2","author":"Dubey","year":"2022","journal-title":"Emerg. Anim. Species"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1016\/j.rvsc.2021.04.017","article-title":"Recent epidemiologic, clinical, and genetic diversity of Toxoplasma gondii infections in non-human primates","volume":"136","author":"Dubey","year":"2021","journal-title":"Res. Vet. Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1177\/10406387211001869","article-title":"Pathologic and immunohistochemical findings in an outbreak of systemic toxoplasmosis in a mob of red kangaroos","volume":"33","author":"Carossino","year":"2021","journal-title":"J. Vet. Diagn. Invest."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1607","DOI":"10.1007\/s10764-008-9317-y","article-title":"Lemur Diversity in Madagascar","volume":"29","author":"Mittermeier","year":"2008","journal-title":"Int. J. Primatol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"8030","DOI":"10.1002\/ece3.6337","article-title":"Genetic population structure of endangered ring-tailed lemurs (Lemur catta) from nine sites in southern Madagascar","volume":"10","author":"Chandrashekar","year":"2020","journal-title":"Ecol. Evol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1089\/fpd.2016.2185","article-title":"Farm Fairs and Petting Zoos: A Review of Animal Contact as a Source of Zoonotic Enteric Disease","volume":"14","author":"Conrad","year":"2017","journal-title":"Foodborne Pathog. Dis."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Denk, D., De Neck, S., Khaliq, S., and Stidworthy, M.F. (2022). Toxoplasmosis in Zoo Animals: A Retrospective Pathology Review of 126 Cases. Animals, 12.","DOI":"10.3390\/ani12050619"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.cimid.2018.10.002","article-title":"Toxoplasma gondii infection in raptors from Italy: Seroepidemiology and risk factors analysis","volume":"60","author":"Gazzonis","year":"2018","journal-title":"Comp. Immunol. Microbiol. Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"442","DOI":"10.1111\/jeu.12688","article-title":"Toxoplasma gondii, Neospora caninum and Encephalitozoon cuniculi in Animals from Captivity (Zoo and Circus Animals)","volume":"66","author":"Silvestre","year":"2019","journal-title":"J. Eukaryot. Microbiol."},{"key":"ref_15","first-page":"357","article-title":"Preimer isolement de Toxoplasma gondii a Madagascar toxoplasmose spontan\u00e9e et exp\u00e9rimentale du Lemur catta","volume":"55","author":"Sureau","year":"1962","journal-title":"Bull. Soc. Pathol. Exot."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1292\/jvms1939.30.341","article-title":"Histopathological observations on two spontaneous cases of toxoplasmosis in the monkey (Lemur catta)","volume":"30","author":"Itakura","year":"1968","journal-title":"Jpn. J. Vet. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"60","DOI":"10.2307\/20094686","article-title":"Acute acquired toxoplasmosis in primates in a zoo","volume":"15","author":"Borst","year":"1984","journal-title":"J. Zoo Anim. Med."},{"key":"ref_18","first-page":"1272","article-title":"Acute death associated with Toxoplasma gondii in ring tailed lemurs","volume":"187","author":"Dubey","year":"1985","journal-title":"J. Am. Vet. Med. Assoc."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"904","DOI":"10.1645\/GE-249R","article-title":"Disseminated toxoplasmosis in a captive ring-tailed lemur (Lemur catta)","volume":"90","author":"Spencer","year":"2004","journal-title":"J. Parasitol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.1177\/1040638711416963","article-title":"Localized toxoplasmosis in a ring-tailed lemur (Lemur catta) causing placentitis, stillbirths, and disseminated fetal infection","volume":"23","author":"Mainez","year":"2011","journal-title":"J. Vet. Diagn Invest."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"9","DOI":"10.5194\/pb-2-9-2015","article-title":"Unique case of disseminated toxoplasmosis and concurrent hepatic capillariasis in a ring-tailed lemur: First case description","volume":"2","author":"Siskos","year":"2015","journal-title":"Primate Biol."},{"key":"ref_22","first-page":"187","article-title":"Multi-locus genotyping of the Toxoplasma gondii isolated from captive ring-tailed lemur (Lemur catta) in China","volume":"38","author":"Yang","year":"2017","journal-title":"Chin. J. Wildl."},{"key":"ref_23","first-page":"167","article-title":"A case of toxoplasmosis in a monkey","volume":"1","author":"Gorovitz","year":"1954","journal-title":"Quart. Isr. Vet. Med. Assoc."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"196","DOI":"10.1016\/S0021-9975(03)00035-5","article-title":"Pathology of toxoplasmosis in captive new world primates","volume":"129","author":"Epiphanio","year":"2003","journal-title":"J. Comp. Pathol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1038\/244301a0","article-title":"Effect of Toxoplasma gondii on the thymus","volume":"244","author":"Huldt","year":"1973","journal-title":"Nature"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1111\/j.1863-2378.2009.01281.x","article-title":"Statistical evaluation of test accuracy studies for Toxoplasma gondii in food animal intermediate hosts","volume":"57","author":"Gardner","year":"2010","journal-title":"Zoonoses Public Health"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/j.vetpar.2005.06.004","article-title":"Sero-epidemiological survey for toxoplasmosis in wild New World monkeys (Cebus spp.; Alouatta caraya) at the Paran\u00e1 river basin, Paran\u00e1 State, Brazil","volume":"133","author":"Garcia","year":"2005","journal-title":"Vet. Parasitol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.vetpar.2006.09.020","article-title":"Seroprevalence of Toxoplasma gondii, Sarcocystis neurona, and Encephalitozoon cuniculi in three species of lemurs from St. Catherines Island, GA, USA","volume":"144","author":"Yabsley","year":"2007","journal-title":"Vet. Parasitol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.vetpar.2017.01.004","article-title":"Seroepidemiology and risk assessment of Toxoplasma gondii infection in captive wild birds and mammals in two zoos in the North of Portugal","volume":"235","author":"Tidy","year":"2017","journal-title":"Vet. Parasitol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.cimid.2019.04.002","article-title":"Serological survey of Toxoplasma gondii in captive nonhuman primates in zoos in Spain","volume":"65","author":"Dubey","year":"2019","journal-title":"Comp. Immunol. Microbiol. Infect. Dis."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Cat\u00e3o-Dias, J.L., Epiphanio, S., and Kierulff, M.C.M. (2013). Neotropical Primates and Their Susceptibility to Toxoplasma gondii: New Insights for an Old Problem. Primates, Pathogens, and Evolution, Springer.","DOI":"10.1007\/978-1-4614-7181-3_9"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1038\/nature08706","article-title":"Mammalian biodiversity on Madagascar controlled by ocean currents","volume":"463","author":"Ali","year":"2010","journal-title":"Nature"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1002\/ajp.20129","article-title":"Preliminary biomedical evaluation of wild ruffed lemurs (Varecia variegata and V. rubra)","volume":"66","author":"Junge","year":"2005","journal-title":"Am. J. Primatol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1638\/1042-7260(2003)34[0016:BEOFRL]2.0.CO;2","article-title":"Biomedical evaluation of free-ranging ring-tailed lemurs (Lemur catta) in Tsimanampetsotsa Strict Nature Reserve, Madagascar","volume":"34","author":"Dutton","year":"2003","journal-title":"J. Zoo Wildl. Med."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Averdam, A., Petersen, B., Rosner, C., Neff, J., Ross, C., Eberle, M., Aujard, F., Munch, C., Schempp, W., and Carrington, M. (2009). A novel system of polymorphic and diverse NK cell receptors in primates. PLoS Genet., 5.","DOI":"10.1371\/journal.pgen.1000688"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1007\/s00251-011-0586-9","article-title":"The IgE gene in primates exhibits extraordinary evolutionary diversity","volume":"64","author":"Wu","year":"2012","journal-title":"Immunogenetics"},{"key":"ref_37","unstructured":"Schwitzer, C., Mittermeier, R.A., Davies, N., Johnson, S., Ratsimbazafy, J., Razafindramanana, J., Louis, E.E., and Rajaobelina, S. (2013). Lemurs of Madagascar: A Strategy for Their Conservation 2013\u20132016, Bristol Conservation and Science Foundation, and Conservation International. IUCN SSC Primate Specialist Group."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"690","DOI":"10.1016\/S0046-8177(81)80170-0","article-title":"Toxoplasma gondii infection of the central nervous system. Use of the peroxidaseantiperoxidase method to demonstrate toxoplasma in formalin fixed, paraffin embedded tissue sections","volume":"12","author":"Conley","year":"1981","journal-title":"Hum. Pathol."},{"key":"ref_39","first-page":"634","article-title":"Comparison of PCR detection methods for B1, P30, and 18S rDNA genes of T. gondii in aqueous humor","volume":"41","author":"Jones","year":"2000","journal-title":"Invest Ophthalmol Vis Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1017\/S0031182009991065","article-title":"Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii","volume":"137","author":"Su","year":"2010","journal-title":"Parasitology"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/10\/1142\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:45:48Z","timestamp":1760143548000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/10\/1142"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,3]]},"references-count":40,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2022,10]]}},"alternative-id":["pathogens11101142"],"URL":"https:\/\/doi.org\/10.3390\/pathogens11101142","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,3]]}}}