Seroepidemiología y alteraciones bioquímicas asociadas con la infección por Neospora caninum en vacas lecheras de la región noreste de Argelia
Resumen
La neosporosis bovina es una de las principales causas de abortos y mortinatalidad en el ganado vacuno, lo que provoca importantes pérdidas económicas en todo el mundo. El objetivo de este estudio fue determinar la seroprevalencia de Neospora caninum, identificar sus posibles factores de riesgo e investigar las alteraciones en determinados parámetros bioquímicos en el ganado vacuno de cinco provincias del noreste de Argelia. Entre marzo de 2022 y abril de 2025, se tomaron muestras aleatorias de 368 vacas pertenecientes a 36 rebaños y se analizaron utilizando un kit ensayo por inmunoabsorción ligado a enzimas indirecto. Los factores de riesgo se determinaron mediante un modelo de regresión logística multivariable. En cuanto a las alteraciones bioquímicas, se analizaron las muestras de suero de 30 vacas seropositivas y 30 seronegativas para determinar los niveles de glucosa, proteína total, albúmina, calcio, fósforo, urea, creatinina, alanina aminotransferasa, aspartato aminotransferasa, gamma- glutamil transferasa, fosfatasa alcalina, lactato deshidrogenasa y β-hidroxibutirato, utilizando métodos de laboratorio estándar. Los valores bioquímicos se compararon estadísticamente y los efectos de la infección por N. caninum se evaluaron mediante modelos lineales generalizados ajustados por factores de confusión. Según los resultados, la prevalencia en el rebaño y en los animales individuales fue del 63,88 % (23/36; IC del 95 %: 46,20 – 79,20) y del 16,30 % (60/368; IC del 95 %: 12,70 – 20,50), respectivamente. A nivel individual, el riesgo de ser seropositivo aumentaba con la edad, los antecedentes de problemas reproductivos, la mastitis y los tipos de vacunas. El uso de la inseminación artificial, la vacunación y el nacimiento de terneros sanos fueron factores protectores. A nivel de rebaño, la cuarentena y la vacunación fueron factores protectores. Las vacas infectadas mostraron niveles séricos significativamente elevados de alanina aminotransferasa, aspartato aminotransferasa, gamma- glutamil transferasa, urea y proteína total y globulina, junto con una disminución significativa del calcio y de la relación albúmina/globulina. Este estudio pone de relieve la amplia diseminación de N. caninum en nuestra población bovina local y aclara los factores de riesgo asociados, así como los trastornos metabólicos y reproductivos que puede provocar.
Descargas
Citas
Dubey JP, Hemphill A, Calero-Bernal R, Schares G. Neosporosis in Animals. [Internet]. 1st Edition. Boca Raton, Florida, USA: CRC Press; 2017. doi: https://doi.org/rh84 DOI: https://doi.org/10.1201/9781315152561-2
Reichel MP, Ayanegui-Alcérreca MA, Gondim LFP, Ellis JT. What is the global economic impact of Neospora caninum in cattle-the billion-dollar question. Int. J. Parasitol. [Internet]. 2013; 43(2):133–142. doi: https://doi.org/f4qz3c DOI: https://doi.org/10.1016/j.ijpara.2012.10.022
McAllister MM, Dubey JP, Lindsay DS, Jolley WR, Wills RA, McGuire AM. Rapid communication: Dogs are definitive hosts of Neospora caninum. Int. J. Parasitol. [Internet]. 1998; 28(9):1473–1479. doi: https://doi.org/bxrjtc DOI: https://doi.org/10.1016/S0020-7519(98)00138-6
King JS, Šlapeta J, Jenkins DJ, Al-Qassab SE, Ellis JT, Windsor PA. Australian dingoes are definitive hosts of Neospora caninum. Int. J. Parasitol. [Internet]. 2010; 40(8):945–950. doi: https://doi.org/dsnqxc DOI: https://doi.org/10.1016/j.ijpara.2010.01.008
Ribeiro CM, Soares IR, Mendes RG, de Santis-Bastos PA, Katagiri S, Zavilenski RB, Porto de Abreu HF, Afreixo V. Meta-analysis of the prevalence and risk factors associated with bovine neosporosis. Trop. Anim. Health Prod. [Internet]. 2019; 51(7):1783–1800. doi: https://doi.org/pjbj DOI: https://doi.org/10.1007/s11250-019-01929-8
Donahoe SL, Lindsay SA, Krockenberger M, Phalen D, Šlapeta J. A review of neosporosis and pathologic findings of Neospora caninum infection in wildlife. Int. J. Parasitol. Parasites Wildl. [Internet]. 2015; 4(2):216–238. doi: https://doi.org/rh85 DOI: https://doi.org/10.1016/j.ijppaw.2015.04.002
Gliga DS, Zumthor JP, Frey CF, Basso W. Enhancing farmer awareness: Vertical transmission of Neospora caninum in aborting cattle and the value of diagnostics tools. Vet. Parasitol. [Internet]. 2025; 334:110403. doi: https://doi.org/rh86 DOI: https://doi.org/10.1016/j.vetpar.2025.110403
Dubey JP, Buxton D, Wouda W. Pathogenesis of bovine neosporosis. J. Comp. Pathol. [Internet]. 2006; 134(4):267–289. doi: https://doi.org/dwjcjp DOI: https://doi.org/10.1016/j.jcpa.2005.11.004
Regidor-Cerrillo J, Xia D, Jiménez-Pelayo L, García-Sánchez M, Collantes-Fernández E, Randle N, Wastling JM, Ortega-Mora LM, Horcajo P. Proteomic characterization of host-pathogen interactions during bovine trophoblast cell line infection by Neospora caninum. Pathogens. [Internet]. 2020; 9(9):749. doi: https://doi.org/rh87 DOI: https://doi.org/10.3390/pathogens9090749
Dos Santos-Hofmeister K, Quillas LJA, da Silva WDM, Moura LSP, Dos Santos-Costa MT, Nakazato L, Mee JF, Souza MA, Pescador CA. Neospora caninum detection in bovine aborted fetuses submitted to the Veterinary Pathology Laboratory (UFMT), Brazil. Vet. Parasitol. Reg. Stud. Reports. [Internet]. 2025; 64:101331. doi: https://doi.org/rh88 DOI: https://doi.org/10.1016/j.vprsr.2025.101331
Erdogan-Bamac O, Haktanir D, Çetinkaya H, Yuzbasioglu-Özturk G, Gurel A, Mete A. Neospora caninum in aborted bovine fetuses in Trakya Region, Turkey histopathological, immunohistochemical and molecular detection. Acta Sci. Vet. [Internet]. 2022; 50:125693. doi: https://doi.org/rh89 DOI: https://doi.org/10.22456/1679-9216.125693
Al-Shaeli SJJ, Ethaeb AM, Gharban HAJ. Molecular and histopathological identification of ovine neosporosis (Neospora caninum) in aborted ewes in Iraq. Vet. World. [Internet]. 2020; 13(3):597–603. doi: https://doi.org/rh9b DOI: https://doi.org/10.14202/vetworld.2020.597-603
de Barros LD, Bogado ALG, Furlan D, de Melo-Jardim A, Okano W, da Silva LC, Sargentin-Pereira CE, Bronkhorst DE, Cardim ST, Garcia JL. Effects of Neospora caninum on reproductive parameters in dairy cows from a closed herd in Brazil. Vet. Parasitol. Reg. Stud. Reports. [Internet]. 2021; 23:100524. doi: https://doi.org/rh9c DOI: https://doi.org/10.1016/j.vprsr.2020.100524
Villa L, Allievi C, Di Cerbo AR, Zanzani SA, Sommariva F, Zanini L, Mortarino M, Manfredi MT. Neospora caninum antibodies in bulk tank milk from dairy cattle herds in Italy in relation to reproductive and productive parameters and spatial analysis. Acta Trop. [Internet]. 2024; 254:107194. doi: https://doi.org/rh9d DOI: https://doi.org/10.1016/j.actatropica.2024.107194
Micheloud JF, Moore DP, Canal AM, Lischinsky L, Hecker YP, Canton GJ, Odriozola E, Odeon AC, Campero CM. First report of congenital Neospora caninum encephalomyelitis in two newborn calves in the Argentinean Pampas. J. Vet. Sci. Technol. [Internet]. 2015; 6(5):251. doi: https://doi.org/rh9f DOI: https://doi.org/10.4172/2157-7579.1000251
Wei XY, An Q, Xue NY, Chen Y, Chen YY, Zhang Y, Zhao GH, Wang CR. Seroprevalence and risk factors of Neospora caninum infection in cattle in China from 2011 to 2020: A systematic review and meta-analysis. Prev. Vet. Med. [Internet]. 2022; 203:105620. doi: https://doi.org/rh9g DOI: https://doi.org/10.1016/j.prevetmed.2022.105620
Lefkaditis M, Mpairamoglou R, Sossidou A, Spanoudis K, Tsakiroglou M. Neospora caninum, a potential cause of reproductive failure in dairy cows from Northern Greece. Vet. Parasitol. Reg. Stud. Reports. [Internet]. 2020; 19:100365. doi: https://doi.org/gqrtxm DOI: https://doi.org/10.1016/j.vprsr.2019.100365
Semango G, Hamilton CM, Kreppel K, Katzer F, Kibona T, Lankester F, Allan KJ, Thomas KN, Claxton JR, Swai ES, Glanville WA, Cleaveland S, Innes EA, Buza J. The seroepidemiology of Neospora caninum in cattle in Northern Tanzania. Front. Vet. Sci. [Internet]. 2019; 6:327. doi: https://doi.org/rh9h DOI: https://doi.org/10.3389/fvets.2019.00327
Abdeltif B, Tennah S, Derdour SY, Temim A, Boufendi H, Ghalmi F. The first study on seroprevalence and risk factors of Neospora caninum infection in pregnant local cows from Northeast Algeria. Vet. World. [Internet]. 2022; 15(2):442–448. doi: https://doi.org/rh9j DOI: https://doi.org/10.14202/vetworld.2022.442-448
Topographic Maps. Free topographic maps, altitude, relief. [Internet]. Prague, Chequia: Topographic-Map.com; [Accessed 24 Nov 2025]. Available in: https://goo.su/W6K59
Climate Data. Climate data for cities worldwide. [Internet]. Berlin, Germany: Climate-Data.org; [Accessed 24 Nov 2025]. Available in: https://goo.su/U3KaS
Ministry of Agriculture and Rural Development (MADR). General Agricultural Census 2024. [Internet]. Algiers: MADR; 2025 [Accessed 24 Dec 2025]. Available in: https://fr.madr.gov.dz/
Thrusfield M. Simple random sampling. In: Thrusfield M, editor. Veterinary Epidemiology. 3rd ed. Oxford, United Kingdom: Blackwell Science; 2007 [Accessed 24 Nov 2025]. p. 231–245. Available in: https://goo.su/Or4qy
Achour K, Ben-Mahdi MH, Akkou M, Teniou R. Seroprevalence of Neospora caninum in dairy cattle farms in Algeria's central northern region. Rev. Sci. Tech. [Internet]. 2012 [Accessed 24 Nov 2025]; 31(3):953–958. Available in: https://goo.su/vbHFH DOI: https://doi.org/10.20506/rst.31.3.2178
Ghalmi F, China B, Ghalmi A, Hammitouche D, Losson B. Study of the risk factors associated with Neospora caninum seroprevalence in Algerian cattle populations. Res. Vet. Sci. [Internet]. 2012; 93(2):655–661. doi: https://doi.org/fz2z7k DOI: https://doi.org/10.1016/j.rvsc.2011.12.015
Miroud K, Benlakehal A, Kaidi R. Seroprevalence of anti-Neospora caninum antibodies in cows of North-Eastern Algeria. Vet. World. [Internet]. 2019; 12(6):765–768. doi: https://doi.org/rh9p DOI: https://doi.org/10.14202/vetworld.2019.765-768
Derdour SY, Hafsi F, Azzag N, Tennah S, Laamari A, China B, Ghalmi F. Prevalence of the main infectious causes of abortion in dairy cattle in Algeria. J. Vet. Res. [Internet]. 2017; 61(3):337–343. doi: https://doi.org/gdt2w4 DOI: https://doi.org/10.1515/jvetres-2017-0044
Waap H, Bärwald A, Nunes T, Schares G. Seroprevalence and risk factors for Toxoplasma gondii and Neospora caninum in cattle in Portugal. Animals. [Internet]. 2022; 12(16):2080. doi: https://doi.org/g5hvrb DOI: https://doi.org/10.3390/ani12162080
Fereig RM, AbouLaila MR, Mohamed SGA, Mahmoud HYAH, Ali AO, Ali AF, Hilali M, Zaid A, Mohamed AEA, Nishikawa Y. Serological detection and epidemiology of Neospora caninum and Cryptosporidium parvum antibodies in cattle in southern Egypt. Acta Trop. [Internet]. 2016; 162:206–211. doi: https://doi.org/f8zb93 DOI: https://doi.org/10.1016/j.actatropica.2016.06.032
Venturoso PJS, Venturoso OJ, Silva GG, Maia MO, Witter R, Aguiar DM, Pacheco TA, Ferreira E, da Costa AJ, dos Santos-Doni TR. Risk factor analysis associated with Neospora caninum in dairy cattle in Western Brazilian Amazon. Rev. Bras. Parasitol. Vet. [Internet]. 2021; 30(1): e023020. doi: https://doi.org/rh9q DOI: https://doi.org/10.1590/s1984-296120201088
Asmare K, Regassa F, Robertson LJ, Skjerve E. Seroprevalence of Neospora caninum and associated risk factors in intensive or semi-intensively managed dairy and breeding cattle of Ethiopia. Vet. Parasitol. [Internet]. 2013; 193(1–3):85–94. doi: https://doi.org/f4sf8n DOI: https://doi.org/10.1016/j.vetpar.2012.11.025
Cao H, Zheng WB, Wang Y, Gao WW, Liu Q, Zhu XQ, Lei YP, Tumen B, Song HY. Seroprevalence of Neospora caninum infection and associated risk factors in cattle in Shanxi Province, north China. Front. Vet. Sci. [Internet]. 2022; 9:1053270. doi: https://doi.org/rh9r DOI: https://doi.org/10.3389/fvets.2022.1053270
Zouagui Z, El Berbri I, El Gourany M, Berrada J. Étude séroépidémiologique des principales maladies infectieuses abortives chez la vache laitière au Maroc. Rev. Maroc. Sci. Agron. Vét. [Internet]. 2024; 12(4):218-222. doi: https://doi.org/rh9s
Amdouni Y, Rjeibi MR, Awadi S, Gharbi M. Molecular identification of Neospora caninum and co-infection with Toxoplasma gondii in genital apparatus of naturally infected cows in North Tunisia. Trop. Anim. Health Prod. [Internet]. 2021; 53(6):528. doi: https://doi.org/gm97zc DOI: https://doi.org/10.1007/s11250-021-02975-x
Dubey JP, Schares G, Ortega-Mora LM. Epidemiology and control of neosporosis and Neospora caninum. Clin. Microbiol. Rev. [Internet]. 2007; 20(2):323–367. doi: https://doi.org/dhtw6r DOI: https://doi.org/10.1128/CMR.00031-06
Selim A, Alshammari A, Gattan HS, Marzok M, Salem M, Al-Jabr OA. Neospora caninum infection in dairy cattle in Egypt: a serosurvey and associated risk factors. Sci. Rep. [Internet]. 2023; 13(1):15489. doi: https://doi.org/rh9t DOI: https://doi.org/10.1038/s41598-023-42538-8
Llano HAB, Guimarães MS, Soares RM, Polo G, Da Silva AC. Seroprevalence and risk factors for Neospora caninum infection in cattle from the eastern Antioquia, Colombia. Vet. Anim. Sci. [Internet]. 2018; 6:69–74. doi: https://doi.org/gqrtxp DOI: https://doi.org/10.1016/j.vas.2018.03.001
Noori M, Rasekh M, Ganjali M, Nourollahi-Fard SR. Seroprevalence of Neospora caninum infection and associated risk factors in cattle of Sistan areas, southeastern Iran in 2016. Iran J. Parasitol. [Internet]. 2019; 14(2):340–346. doi: https://doi.org/rh9v DOI: https://doi.org/10.18502/ijpa.v14i2.1149
Woodbine KA, Medley GF, Moore SJ, Ramirez-Villaescusa A, Mason S, Green LE. A four year longitudinal seroepidemiology study of Neospora caninum in adult cattle from 114 cattle herds in south west England: associations with age, herd and dam-offspring pairs. BMC Vet. Res. [Internet]. 2008; 4(1):35. doi: https://doi.org/ft7d99 DOI: https://doi.org/10.1186/1746-6148-4-35
Thurmond MC, Hietala SK. Culling associated with Neospora caninum infection in dairy cows. Am. J. Vet. Res. [Internet]. 1996; 57(11):1559–1562. doi: https://doi.org/rh9w DOI: https://doi.org/10.2460/ajvr.1996.57.11.1559
Peregrine AS, Duffield TF, Wideman G, Kelton D, Hobson J, Cramer G, Hietala SK. Udder health in dairy cattle infected with Neospora caninum. Prev. Vet. Med. [Internet]. 2004; 64(2–4):101–112. doi: https://doi.org/fk646d DOI: https://doi.org/10.1016/j.prevetmed.2004.05.007
Lagomarsino H, Scioli A, Rodríguez A, Armendano J, Fiorani F, Bence Á, García J, Hecker Y, Gual I, Cantón G, Odeón A, Moore D, Campero CM. Controlling endemic Neospora caninum-related abortions in a dairy herd from Argentina. Front. Vet. Sci. [Internet]. 2019; 6:446. doi: https://doi.org/rh9x DOI: https://doi.org/10.3389/fvets.2019.00446
Marugan-Hernandez V. Neospora caninum and bovine neosporosis: current vaccine research. J. Comp. Pathol. [Internet]. 2017; 157(2–3):193–200. doi: https://doi.org/rh9z DOI: https://doi.org/10.1016/j.jcpa.2017.08.001
Cavirani S, Cabassi CS, Taddei S, Donofrio G, Bottarelli E. Association between Neospora caninum antibodies and blue tongue vaccination in dairy cows. Vet. Res. Commun. [Internet]. 2005; 29(S2):233–236. doi: https://doi.org/c5258c DOI: https://doi.org/10.1007/s11259-005-0050-0
Roszak K, Roy K, Sobocinska J, Spisz P, Jedrzejewski T, Wrotek S. Endotoxin's impact on organism: from immune activation to tolerance and beyond. J. Clin. Med. [Internet]. 2025; 14(18):6478. doi: https://doi.org/rh92 DOI: https://doi.org/10.3390/jcm14186478
Cozzi G, Ravarotto L, Gottardo F, Stefani AL, Contiero B, Moro L, Brscic M, Dalvit P. Short communication: Reference values for blood parameters in Holstein dairy cows: effects of parity, stage of lactation, and season of production. J. Dairy Sci. [Internet]. 2011; 94(8):3895–3901. doi: https://doi.org/cdj4bn DOI: https://doi.org/10.3168/jds.2010-3687
Zaitsev SY, Bogolyubova NV, Zhang X, Brenig B. Biochemical parameters, dynamic tensiometry and circulating nucleic acids for cattle blood analysis: a review. PeerJ. [Internet]. 2020; 8:e8997. doi: https://doi.org/rh93 DOI: https://doi.org/10.7717/peerj.8997
Hassan-Abdullah S, Jamal-Nasrulla O, Ismael-Dana O, Othman-Dyary H, Hasanvand M. Ovine toxoplasmosis sero-status, risk factors analysis, and estimation of haematological and serum biochemical alterations. Vet. Med. Sci. [Internet]. 2025; 11(1):e70220. doi: https://doi.org/rh94 DOI: https://doi.org/10.1002/vms3.70220
Alekish MO, Talafha AQ, Alshehabat MA, Ismail ZAB. Relationships between certain metabolic diseases and selected serum biochemical parameters in seropositive dairy cows against Neospora caninum infection in different stages of lactation. Ann. Parasitol. [Internet]. 2017; 63(2):99–103. doi: https://doi.org/rh95
Eder K, Grundmann SM. Vitamin D in dairy cows: metabolism, status and functions in the immune system. Arch. Anim. Nutr. [Internet]. 2022; 76(1):1–33. doi: https://doi.org/rh96 DOI: https://doi.org/10.1080/1745039X.2021.2017747
Carlstedt E, Ridefelt P, Lind L, Rastad J. Interleukin-6 induced suppression of bovine parathyroid hormone secretion. Biosci. Rep. [Internet]. 1999; 19(1):35–42. doi: https://doi.org/cpk45h DOI: https://doi.org/10.1023/A:1020146023812
Gual I, Campero LM, Hecker YP, Regidor-Cerrillo J, Leunda MR, Odeón AC, Moore DP, Campero CM, de Echaide ST, Echaide IE, Estein SM, Ortega-Mora LM. Parasitemia and associated immune response in pregnant and nonpregnant beef cows naturally infected with Neospora caninum. Front. Vet. Sci. [Internet]. 2022; 9:905271. doi: https://doi.org/rh97 DOI: https://doi.org/10.3389/fvets.2022.905271
Appelt MA, Da Silva AS, Cazarotto CJ, Machado G, Rodrigues RS, Norbury LJ, Mendes RE, Baldissera MD, Alba DF, Gris A. Cholinesterase as an inflammatory marker of subclinical infection of dairy cows infected by Neospora caninum and risk factors for disease. Comp. Immunol. Microbiol. Infect. Dis. [Internet]. 2019; 66:101330. doi: https://doi.org/rh98 DOI: https://doi.org/10.1016/j.cimid.2019.101330
