{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T18:21:00Z","timestamp":1788891660290,"version":"build-2803163510"},"reference-count":54,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2020,3,22]],"date-time":"2020-03-22T00:00:00Z","timestamp":1584835200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>One hundred twenty-four water buffaloes (Bubalus bubalis) originating from 9 farms located in southern Italy were tested to investigate simultaneously, for the first time, the seroprevalence of the protozoa Neospora caninum, Toxoplasma gondii and Besnoitia besnoiti by ELISA tests and to evaluate the clinical findings potentially associated to the presence of these aborting parasitic pathogens. Twenty-five of 124 buffaloes (20.2%) were positive for N. caninum, while 17\/124 (13.7%) for T. gondii. No buffalo showed specific antibodies for B. besnoiti. Nineteen of 124 animals (15.3%) were found seropositive for both T. gondii and N. caninum. The univariate statistical analysis showed that the seroprevalence of N. caninum is significantly associated with abortion and presence of retained foetal membranes, while the seroprevalence of T. gondii is significantly associated with an increase of days open. The logistic regression models showed that the co-infection by N. caninum and T. gondii strengthened the abortive effects (OR = 7.330) and showed further negative effects on the parameter embryonic death (OR = 2.607). The outcome revealed herein represents a high exposure of N. caninum and T. gondii in water buffaloes with reproduction disorders that deserves attention for both economic reasons, animal health and welfare.<\/jats:p>","DOI":"10.3390\/ani10030532","type":"journal-article","created":{"date-parts":[[2020,3,24]],"date-time":"2020-03-24T07:16:08Z","timestamp":1585034168000},"page":"532","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Seroprevalence and Clinical Outcomes of Neospora caninum, Toxoplasma gondii and Besnoitia besnoiti Infections in Water Buffaloes (Bubalus bubalis)"],"prefix":"10.3390","volume":"10","author":[{"given":"Lavinia","family":"Ciuca","sequence":"first","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4993-0511","authenticated-orcid":false,"given":"Giuliano","family":"Borriello","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonio","family":"Bosco","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5212-1483","authenticated-orcid":false,"given":"Luigi","family":"D\u2019Andrea","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giuseppe","family":"Cringoli","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5518-5378","authenticated-orcid":false,"given":"Paolo","family":"Ciaramella","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Paola","family":"Maurelli","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6947-0287","authenticated-orcid":false,"given":"Antonio","family":"Di Loria","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura","family":"Rinaldi","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jacopo","family":"Guccione","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples Federico II, Via Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,3,22]]},"reference":[{"key":"ref_1","unstructured":"(2020, February 24). Pdo Buffalo Mozzarella Drives Italian Cheese Export. Available online: https:\/\/news.italianfood.net\/2017\/02\/07\/pdo-buffalo-mozzarella-drives-italian-cheese-export\/."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"15850","DOI":"10.1038\/s41598-019-52063-2","article-title":"Proteomic changes in the milk of water bufaloes (Bubalus bubalis) with subclinical mastitis due to intramammary infection by Staphylococcus aureus and by non-aureus staphylococci","volume":"9","author":"Pisanu","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"456","DOI":"10.29261\/pakvetj\/2018.073","article-title":"External skeletal fixation for surgical repair of a bilateral mandible fracture in a Mediterranean Buffalo","volume":"38","author":"Guccione","year":"2018","journal-title":"Pak. Vet. J."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Cagnardi, P., Guccione, J., Villa, R., D\u2019Andrea, L., Di Loria, A., Ferrante, M.C., Borriello, G., Zicarelli, L., and Ciaramella, P. (2017). Clinical efficacy and pharmacokinetics of meloxicam in Mediterranean buffalo calves (Bubalus bubalis). PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0187252"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e000674","DOI":"10.1136\/vetreccr-2018-000674","article-title":"Detection of Treponema pedis associated with digital dermatitis in Mediterranean buffalo (Bubalus bubalis)","volume":"6","author":"Guccione","year":"2018","journal-title":"Vet. Rec. Case Rep."},{"key":"ref_6","first-page":"1","article-title":"Mastitis in Mediterranean Buffaloes","volume":"2","author":"Guccione","year":"2017","journal-title":"Dairy Vet. Sci. J."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1017\/S0022029919000074","article-title":"Validation of a noseband pressure sensor algorithm as a tool for evaluation of feeding behaviour in dairy Mediterranean buffalo (Bubalus Bubalis)","volume":"86","author":"Guccione","year":"2019","journal-title":"J. Dairy Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1136\/vr.161.9.310","article-title":"Molecular detection of Leptospira species in aborted fetuses of water buffalo","volume":"1","author":"Marianelli","year":"2007","journal-title":"Vet. Rec."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1017\/S0031182017000063","article-title":"Importance of serological cross-reactivity among Toxoplasma gondii, Hammondia spp., Neospora spp., Sarcocystis spp. and Besnoitia besnoiti","volume":"144","author":"Gondim","year":"2017","journal-title":"J. Parasitol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1007\/s11250-013-0522-0","article-title":"Evidence for bovine besnoitiosis in Egypt\u2014First serosurvey of Besnoitia besnoiti in cattle and water buffalo (Bubalus bubalis) in Egypt","volume":"46","author":"Ashmawy","year":"2014","journal-title":"Trop. Anim. Health Prod."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1590\/S1984-29612015066","article-title":"Risk factors for Toxoplasma gondii and Neospora caninum seropositivity in buffaloes in Paraiba State, Brazil","volume":"24","author":"Brasil","year":"2015","journal-title":"Rev. Bras. Parasitol. Vet."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/j.rvsc.2013.04.008","article-title":"Bovine neosporosis: Clinical and practical aspects","volume":"95","year":"2013","journal-title":"Res. Vet. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1016\/j.ijpara.2017.08.003","article-title":"Advances in the diagnosis of bovine besnoitiosis: Current options and applications for control","volume":"47","author":"Ferre","year":"2017","journal-title":"Int. J. Parasitol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1016\/j.cvfa.2012.07.007","article-title":"Ruminant abortion diagnostics. Review","volume":"28","author":"Holler","year":"2012","journal-title":"Vet. Clin. North Am. Food Anim. Pract."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1556\/1886.2017.00029","article-title":"Seroepidemiology of Infection with Neospora Caninum, Leptospira, and Bovine Herpesvirus Type 1 in Water Buffaloes (Bubalus Bubalis) in Veracruz, Mexico","volume":"7","year":"2017","journal-title":"Eur. J. Microbiol. Immunol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1016\/j.ijppaw.2018.08.002","article-title":"Exposure to Neospora spp. and Besnoitia spp. in wildlife from Israel","volume":"7","author":"Mazuz","year":"2018","journal-title":"Int. J. Parasitol. Parasites Wildl."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.cimid.2017.05.005","article-title":"Serological survey of Neospora caninum and Toxoplasma gondii in cattle (Bos indicus) and water buffaloes (Bubalus bubalis) in ten provinces of Brazil","volume":"52","author":"Nicolinoa","year":"2017","journal-title":"Comp. Immunol. Microbiol. Infect. Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/S0304-4017(00)00239-9","article-title":"Neosporosis in water buffalo (Bubalus bubalis) in Southern Italy","volume":"91","author":"Guarino","year":"2000","journal-title":"Vet. Parasitol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.2478\/s11686-014-0201-y","article-title":"PCR detection of Neospora caninum in water buffalo foetal tissues","volume":"59","author":"Auriemma","year":"2014","journal-title":"Acta Parasitol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.vetpar.2003.10.008","article-title":"Seroprevalence and associated risk factors of neosporosis in beef and dairy cattle in Italy","volume":"118","author":"Otranto","year":"2003","journal-title":"Vet. Parasitol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.vetpar.2004.05.022","article-title":"Seroprevalence of Neospora spp. in asymptomatic horses in Italy","volume":"123","author":"Ciaramella","year":"2004","journal-title":"Vet. Parasitol."},{"key":"ref_22","first-page":"201","article-title":"Seroprevalence and risk factors of Neospora spp. in donkeys from Southern Italy","volume":"15","author":"Guccione","year":"2013","journal-title":"Vet. Parasitol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"754","DOI":"10.1136\/vr.148.24.754","article-title":"Prevalence of Neospora caninum antibodies in wild ruminants from the Italian Alps","volume":"148","author":"Ferroglio","year":"2001","journal-title":"Vet. Rec."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1304","DOI":"10.2174\/1568026618666181002113617","article-title":"Treatment of Toxoplasmosis and Neosporosis in Farm Ruminants: State of Knowledge and Future Trends","volume":"18","author":"Ferre","year":"2018","journal-title":"Curr. Top. Med. Chem."},{"key":"ref_25","unstructured":"Dubey, J.P. (2010). Toxoplasmosis of Animals and Humans, CRC Press, Taylor and Francis Group. [2nd ed.]."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"978","DOI":"10.1016\/j.ijid.2010.05.018","article-title":"Toxoplasma gondii infection in first-episode and in patient individuals with schizophrenia","volume":"14","author":"Hamidinejat","year":"2010","journal-title":"Int. J. Infect. Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"981","DOI":"10.20506\/rst.36.3.2730","article-title":"Seroprevalence of Toxoplasma gondii in South Asian countries","volume":"36","author":"Khan","year":"2017","journal-title":"Rev. Sci. Tech."},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Alvarado-Esquivel, C., Romero-Salas, D., Garc\u00eda-V\u00e1zquez, Z., Cruz-Romero, A., Peniche-Carde\u00f1a, A., Ibarra-Priego, N., Aguilar-Dom\u00ednguez, M., P\u00e9rez-de-Le\u00f3n, A.A., and Dubey, J.P. (2014). Seroprevalence of Toxoplasma gondii infection in water buffaloes (Bubalus bubalis) in Veracruz State, Mexico and its association with climatic factors. BMC Vet. Res., 10.","DOI":"10.1186\/s12917-014-0232-5"},{"key":"ref_29","first-page":"275","article-title":"Seroprevalence of Toxoplasma gondii in water buffaloes (Bubalus bubalis) in South-West of Iran","volume":"27","author":"Hamidinejat","year":"2010","journal-title":"Trop. Biomed."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2695","DOI":"10.1007\/s00436-019-06396-6","article-title":"Toxoplasma gondii in water buffaloes (Bubalus bubalis) from Romania: What is the importance for public health?","volume":"118","author":"Blaga","year":"2019","journal-title":"Parasitol. Res."},{"key":"ref_31","first-page":"225","article-title":"Indagini siero-epidemiologiche sulla diffusione della toxoplasmosi nei bufali in Campania","volume":"26","author":"Persechino","year":"1980","journal-title":"Acta Med. Vet."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1186\/1756-3305-6-191","article-title":"Seroprevalence and risk factors of toxoplasmosis in cattle from extensive and semi-intensive rearing systems at Zona da Mata, Minas Gerais state, Southern Brazil","volume":"25","author":"Fajardo","year":"2013","journal-title":"Parasites Vectors"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/j.vetpar.2011.01.027","article-title":"Exploring the life cycle of Besnoitia besnoiti\u2014Experimental infection of putative definitive and intermediate host species","volume":"178","author":"Basso","year":"2011","journal-title":"Vet. Parasitol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1017\/S0031182014000729","article-title":"Dynamics of Besnoitia besnoiti infection in cattle","volume":"141","author":"Shkap","year":"2014","journal-title":"Parasitology"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"European Food Safety Authority (EFSA) (2010). Bovine Besnoitiosis: An emerging disease in Europe. EFSA J., 8, 1499.","DOI":"10.2903\/j.efsa.2010.1499"},{"key":"ref_36","first-page":"407","article-title":"A century of bovine besnoitiosis: An unknown disease re-emerging in Europe","volume":"8","author":"Frey","year":"2013","journal-title":"Trends Parasitol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1805","DOI":"10.1007\/s00436-012-3241-y","article-title":"First cross-sectional serological survey on Besnoitia besnoiti in cattle in Italy","volume":"112","author":"Rinaldi","year":"2013","journal-title":"Parasitol. Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"9236","DOI":"10.3168\/jds.2019-16515","article-title":"Effect of student transrectal palpation on early pregnancy loss in dairy cattle","volume":"102","author":"Bond","year":"2019","journal-title":"J. Dairy Sci."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Green, M. (2012). Managing herd reproduction. Dairy Herd Health, CABI International.","DOI":"10.1079\/9781845939977.0000"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1206","DOI":"10.1016\/j.theriogenology.2015.06.022","article-title":"Postpartum uterine diseases and their impacts on conception and days open in dairy herds in Italy","volume":"15","author":"Toni","year":"2015","journal-title":"Theriogenology"},{"key":"ref_41","unstructured":"Noel, A. (2000). Introduction to the Logistic Regression Model. Applied Logistic Regression, John Wiley & Sons, Inc."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1111\/j.1467-842X.1961.tb00058.x","article-title":"The combination of probabilities: An application of orthonormal functions","volume":"3","author":"Lancaster","year":"1961","journal-title":"Aust. J. Stat."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.vetpar.2015.08.008","article-title":"A review of Neospora caninum in water buffalo (Bubalus bubalis)","volume":"212","author":"Reichel","year":"2015","journal-title":"Vet. Parasitol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1007\/s00436-014-4178-0","article-title":"Abortion and foetal lesions induced by Neospora caninum in experimentally infected water buffalos (Bubalus bubalis)","volume":"114","author":"Chryssafidis","year":"2015","journal-title":"Parasitol. Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/j.vetpar.2004.09.025","article-title":"Risk factors associated with Neospora caninum abortion in Ontario Holstein dairy herds","volume":"127","author":"Hobson","year":"2005","journal-title":"Vet. Parasitol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/S0378-4320(00)00117-2","article-title":"Neosporosis in cattle","volume":"60\u201361","author":"Anderson","year":"2000","journal-title":"Anim. Reprod. Sci."},{"key":"ref_47","unstructured":"Radostis, O.M., Gay, C.C., Hinchcliff, K.W., and Constable, P.D. (2007). Diseases associated with protozoa-chapter. Veterinary Medicine, Elsevier Saunders. [10th ed.]."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1645\/0022-3395(2002)088[1247:IOVTGF]2.0.CO;2","article-title":"Isolation of viable Toxoplasma gondii from naturally infected aborted bovine fetuses","volume":"88","author":"Canada","year":"2002","journal-title":"J. Parasitol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1174","DOI":"10.1645\/GE-1556.1","article-title":"Serological Survey of Antibodies to Toxoplasma gondii in Sheep, Cattle, and Buffaloes in Punjab, India","volume":"94","author":"Sharma","year":"2008","journal-title":"J. Parasitol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1016\/j.vetpar.2008.02.016","article-title":"Sensitivity and specificity of various serological tests for the detection of Toxoplasma gondii infection in naturally infected sheep","volume":"153","author":"Shaapan","year":"2008","journal-title":"Vet. Parasitol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/j.vetpar.2014.04.011","article-title":"Neospora caninum serostatus is affected by age and species variables in cohabiting water buffaloes and beef cattle","volume":"203","author":"Moore","year":"2014","journal-title":"Vet. Parasitol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1111\/j.1865-1682.2012.01318.x","article-title":"An inter-laboratory comparative study of serological tools employed in the diagnosis of Besnoitia besnoiti infection in bovines","volume":"60","author":"Schares","year":"2013","journal-title":"Transbound. Emerg. Dis."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.vetpar.2013.07.033","article-title":"Serological diagnosis of bovine neosporosis: A comparative study of commercially available ELISA tests","volume":"198","year":"2013","journal-title":"Vet. Parasitol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.vetpar.2007.02.019","article-title":"Toxoplasma gondii infections in sheep in Sicily, southern Italy","volume":"146","author":"Vesco","year":"2007","journal-title":"Vet. Parasitol."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/10\/3\/532\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:10:32Z","timestamp":1760173832000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/10\/3\/532"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,3,22]]},"references-count":54,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2020,3]]}},"alternative-id":["ani10030532"],"URL":"https:\/\/doi.org\/10.3390\/ani10030532","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,3,22]]}}}