Seroprevalence of Toxoplasma gondii in Iberian pig sows

  • Alba Pablos-Tanarro
  • Luis Miguel Ortega-Mora
  • Antonio Palomo
  • Francisco Casasola
  • Ignacio Ferre
Original Paper
  • 56 Downloads

Abstract

The objective of the present study was to investigate the seroprevalence of Toxoplasma gondii infection in Iberian sows reared in extensive and intensive management conditions and to compare two serologic techniques used for diagnosis. In addition, some possible risk factors associated with the presence of serum antibodies to T. gondii were also studied. Serum samples were collected from 2492 Iberian sows on 14 pig farms. Three types of management systems were included, traditional extensive outdoor farms (five farms), intensive farms with outdoor access (n = 4), and conventional intensive indoor farms (n = 5). The presence of serum antibodies to T. gondii was evaluated by two commercially available tests: an indirect enzyme-linked immunosorbent assay (ELISA) and a direct agglutination test (DAT). Serum antibodies against T. gondii were detected in 237 sows (9.5%) by at least one of the techniques used. The mean seroprevalence of toxoplasmosis in Iberian sows was 5.8% by ELISA and 8.9% by DAT. An agreement kappa-value of 0.68 (95%, CI = 0.63–0.74) was found between both tests. The results from this study suggest that the prevalence of T. gondii antibodies among Iberian sows seems to be moderate-low. The presence of serum antibodies against T. gondii in Iberian sows was associated to an extensive management system and low-level facilities of the farm, sow number (> 1000 animals), presence of cats, absence of rodent control and bird-proof nets in windows, well-water source, feed sources and storage (from the same farm and not stored in silo), absence of fences, and low farm worker qualification.

Keywords

Seroprevalence Epidemiology Risk factors Toxoplasma gondii Pig Iberian sow 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Belluco S, Mancin M, Conficoni D, Simonato G, Pietrobelli M, Ricci A (2016) Investigating the determinants of Toxoplasma gondii prevalence in meat: a systematic review and meta-regression. PloS One 11(4):e0153856.  https://doi.org/10.1371/journal.pone.0153856 eCollection 2016CrossRefPubMedPubMedCentralGoogle Scholar
  2. Damriyasa IM, Bauer C, Edelhofer R, Failing K, Lind P, Petersen E, Schares G, Tenter AM, Volmer R, Zahner H (2004) Cross-sectional survey in pig breeding farms in Hesse, Germany: seroprevalence and risk factors of infections with Toxoplasma gondii, Sarcocystis spp. and Neospora caninum in sows. Vet Parasitol 126:271–286CrossRefPubMedGoogle Scholar
  3. Davies PR, Morrow WEM, Deen J, Gamble HR, Patton S (1998) Seroprevalence of Toxoplasma gondii and Trichinella spiralis in finishing swine raised in different production systems in North Carolina, USA. Prev Vet Med 36:67–76CrossRefPubMedGoogle Scholar
  4. De Berardinis A, Paludi D, Pennisi L, Vergara A (2017) Toxoplasma gondii, a foodborne pathogen in the swine production chain from a European perspective. Foodborne Pathog Dis 14:637–648CrossRefPubMedGoogle Scholar
  5. Djokic V, Fablet C, Blaga R, Rose N, Perret C, Djurkovic-Djakovic O, Boireau P, Durand B (2016a) Factors associated with Toxoplasma gondii infection in confined farrow-to-finish pig herds in western France: an exploratory study in 60 herds. Parasit Vectors 9:466.  https://doi.org/10.1186/s13071-016-1753-5 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Djokic V, Blaga R, Aubert D, Durand B, Perret C, Geers R, Ducry T, Vallee I, Djurkovic-Djakovic O, Mzabi A, Villena I, Boireau P (2016b) Toxoplasma gondii infection in pork produced in France. Parasitology 143:557–567CrossRefPubMedGoogle Scholar
  7. Dubey JP (2010) Toxoplasmosis of animals and humans, second edn. CRC Press, Boca Raton. FloridaGoogle Scholar
  8. Dubey JP (2009) Toxoplasmosis in pigs-the last 20 years. Vet Parasitol 164:89–103CrossRefPubMedGoogle Scholar
  9. Dubey JP, Thulliez P, Weigel RM, Andrews CD, Lind P, Powell EC (1995) Sensitivity and specificity of various serologic tests for detection of Toxoplasma gondii infection in naturally infected sows. Am J Vet Res 56:1030–1036PubMedGoogle Scholar
  10. Dubey JP, Gamble HR, Hill D, Sreekumar C, Romand S, Thulliez P (2002) High prevalence of viable Toxoplasma gondii infection in market weight pigs from a farm in Massachusetts. J Parasitol 88:1234–1238CrossRefPubMedGoogle Scholar
  11. Dubey JP, Hill DE, Sundar N, Velmurugan GV, Bandini LA, Kwok OCH, Pierce V, Kelly K, Dulin M, Thulliez P, Iwueke C, Su C (2008) Endemic toxoplasmosis in pigs on a farm in Maryland: isolation and genetic characterization of Toxoplasma gondii. J Parasitol 94:36–41CrossRefPubMedGoogle Scholar
  12. Gamble HR, Dubey JP, Lambillotte DN (2005) Comparison of a commercial ELISA with the modified agglutination test for detection of Toxoplasma infection in the domestic pig. Vet Parasitol 128:177–181CrossRefPubMedGoogle Scholar
  13. García-Bocanegra I, Dubey JP, Simón-Grifé M, Cabezón O, Casal J, Allepuz A, Napp S, Almería S (2010a) Seroprevalence and risk factors associated with Toxoplasma gondii infection in pig farms from Catalonia, north-eastern Spain. Res Vet Sci 89:85–87CrossRefPubMedGoogle Scholar
  14. García-Bocanegra I, Simón-Grifé M, Dubey JP, Casal J, Martín GE, Cabezón O, Perea A, Almería S (2010b) Seroprevalence and risk factors associated with Toxoplasma gondii in domestic pigs from Spain. Parasitol Int 59:421–426CrossRefPubMedGoogle Scholar
  15. Garcia JL, Navarro IT, Vidotto O, Gennari SM, Machado RZ, da Luz Pereira AB, Sinhorini IL (2006) Toxoplasma gondii: comparison of a rhoptry-ELISA with IFAT and MAT for antibody detection in sera of experimentally infected pigs. Exp Parasitol 113:100–105CrossRefPubMedGoogle Scholar
  16. Gebreyes WA, Bahnson PB, Funk JA, McKean J, Patchanee P (2008) Seroprevalence of Trichinella, Toxoplasma, and Salmonella in antimicrobial-free and conventional swine production systems. Foodborne Pathog Dis 5:199–203CrossRefPubMedGoogle Scholar
  17. Guo M, Mishra A, Buchanan RL, Dubey JP, Hill DE, Gamble HR, Jones JL, Pradhan AK (2016) A systematic meta-analysis of Toxoplasma gondii prevalence in food animals in the United States. Foodborne Pathog Dis 13:109–118CrossRefPubMedGoogle Scholar
  18. Hernández M, Gómez-Laguna J, Tarradas C, Luque I, García-Valverde R, Reguillo L, Astorga RJ (2014) A serological survey of Brucella spp., Salmonella spp., Toxoplasma gondii and Trichinella spp. in Iberian fattening pigs reared in free-range systems. Transbound Emerg Dis 61:477–481CrossRefPubMedGoogle Scholar
  19. Herrero L, Gracia MJ, Pérez-Arguillué C, Lázaro R, Herrera M, Herrera A, Bayarri S (2016) Toxoplasma gondii: pig seroprevalence, associated risk factors and viability in fresh pork meat. Vet Parasitol 224:52–59CrossRefPubMedGoogle Scholar
  20. Hill DE, Sreekumar C, Dubey JP, Lunney JK, Gamble HR (2006) Comparison of detection methods for Toxoplasma gondii in naturally and experimentally infected swine. Vet Parasitol 141:9–17CrossRefPubMedGoogle Scholar
  21. Kijlstra A, Eissen OA, Cornelissen J, Munniksma K, Eijck I, Kortbeek T (2004) Toxoplasma gondii infection in animal-friendly pig production systems. Invest Ophthalmol Vis Sci 45:3165–3169CrossRefPubMedGoogle Scholar
  22. Kijlstra A, Meerburg B, Cornelissen J, De Craeye S, Vereijken P, Jongert E (2008) The role of rodents and shrews in the transmission of Toxoplasma gondii to pigs. Vet Parasitol 156:183–190CrossRefPubMedGoogle Scholar
  23. Lehmann T, Graham DH, Dahl E, Sreekumar C, Launer F, Corn JL, Gamble HR, Dubey JP (2003) Transmission dynamics of Toxoplasma gondii on a pig farm. Infect Genet Evolution 3:135–141CrossRefGoogle Scholar
  24. Limon G, Beauvais W, Dadios N, Villena I, Cockle C, Blaga R, Guitian J (2017) Cross-sectional study of Toxoplasma gondii infection in pig farms in England. Foodborne Pathog Dis 14:269–281CrossRefPubMedGoogle Scholar
  25. Meerburg BG, van Riel JW, Cornelissen JB, Kijlstra A, Mul MF (2006) Cats and goat whey associated with Toxoplasma gondii infection in pigs. Vector-Borne Zoonotic Dis 6:266–274CrossRefPubMedGoogle Scholar
  26. Papatsiros VG, Athanasiou LV, Stougiou D, Papadopoulos E, Maragkakis GG, Katsoulos PD, Lefkaditis M, Kantas D, Tzica ED, Tassis PD, Boutsini S (2016) Cross-sectional serosurvey and risk factors associated with the presence of Toxoplasma gondii antibodies in pigs in Greece. Vector Borne Zoonotic Dis 16:48–53CrossRefPubMedGoogle Scholar
  27. Pastiu AI, Gyöke A, Blaga R, Mircean V, Rosenthal BM, Cozma V (2013) In Romania, exposure to Toxoplasma gondii occurs twice as often in swine raised for familial consumption as in hunted wild boar, but occurs rarely, if ever, among fattening pigs raised in confinement. Parasitol Res 112:2403–2407CrossRefPubMedGoogle Scholar
  28. Poljak Z, Dewey CE, Friendship RM, Martin SW, Christensen J, Ojkic D, Wu J, Chow E (2008) Pig and herd level prevalence of Toxoplasma gondii in Ontario finisher pigs in 2001, 2003, and 2004. Can J Vet Res 72:303–310PubMedPubMedCentralGoogle Scholar
  29. Steinparzer R, Reisp K, Grünberger B, Köfer J, Schmoll F, Sattler T (2015) Comparison of different commercial serological tests for the detection of Toxoplasma gondii antibodies in serum of naturally exposed pigs. Zoonoses Public Health 62:119–124CrossRefPubMedGoogle Scholar
  30. van der Giessen J, Fonville M, Bouwknegt M, Langelaar M, Vollema A (2007) Seroprevalence of Trichinella spiralis and Toxoplasma gondii in pigs from different housing systems in The Netherlands. Vet Parasitol 148:371–374CrossRefPubMedGoogle Scholar
  31. Villari S, Vesco G, Petersen E, Crispo A, Buffolano W (2009) Risk factors for toxoplasmosis in pigs bred in Sicily, southern Italy. Vet Parasitol 161:1–8CrossRefPubMedGoogle Scholar
  32. Wallander C, Frössling J, Dórea FC, Uggla A, Vagsholm I, Lundén A (2016) Pasture is a risk factor for Toxoplasma gondii infection in fattening pigs. Vet Parasitol 224:27–32CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.SALUVET Group, Department of Animal Health, Faculty of VeterinaryComplutense UniversityMadridSpain
  2. 2.SETNA NUTRICIÓN SAU-NEOVIAMadridSpain

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