Abstract
Purpose
This study aimed to estimate the prevalence and identify the risk factors associated with the higher in-herd T. gondii seroprevalence in dairy cows in 37 farms in southern Minas Gerais, Southeastern Brazil.
Methods
Serum samples from 1,105 dairy cows were subjected to an indirect fluorescence antibody test (IFAT 1:64) for anti-T. gondii IgG. The association existing between possible risk factors at the herd level and the seroprevalence were verified through Generalized Estimating Equation (GEE) multiple logistic regression models.
Results
Anti-T. gondii antibodies were observed in 31.4% of the cows (347; 95% CI= 28.7–34.2) and on 100% of the farms (37; 95% CI= 90.6–100.0%), indicating that all properties possessed at least one seropositive animal. For univariate analysis, herds with seroprevalence were categorized as greater and less than 30% as the outcome. The "breeding of Holstein Friesian cows" (p= 0.016, OR= 6.667, 95% CI= 1.500–29.628) and in an "intensive system" (p= 0.013, OR= 6.120, 95% CI= 1.394–26.876) increased the chance of the herd seroprevalence being greater than 30% by approximately six-fold. However, these variables did not exhibit a significant association (p >0.05) in the Generalized Estimating Equations (GEE) logistic regression model.
Conclusions
The results demonstrate that T. gondii infection is widespread among dairy cows in the south of Minas Gerais, with a wide environmental dispersion of the parasite on farms in this region.
Similar content being viewed by others
References
Albuquerque GR, Munhoz AD, Teixeira M, Flausino W, Medeiros S, Lopes CWG (2011) Risk factors associated with Toxoplasma gondii infection in dairy cattle, State of Rio de Janeiro. Pesquisa Veterinária Brasileira 31:287–290
Amdouni Y, Rjeibi MR, Rouatbi M, Amairia S, Awadi S, Gharbi M (2017) Molecular detection of Toxoplasma gondii infection in slaughtered ruminants (sheep, goats and cattle) in Northwest Tunisia. Meat Sci 133:180–184
Aspinall TV, Marlee D, Hyde JE, Sims PF (2002) Prevalence of Toxoplasma gondii in commercial meat products as monitored by polymerase chain reaction-food for thought. Int J Parasitol 32:1193–1199
Bañales P, Fernandez L, Repiso MV, Gil A, Dargatz DA, Osawa T (2006) A nationwide survey on seroprevalence of Neospora caninum in beef cattle in Uruguay. Vet Parasitol 139:15–20
Bártová E, Sedlák K, Budíková M (2015) A study of Neospora caninum and Toxoplasma gondii antibody seroprevalence in healthy cattle in the Czech Republic. Ann Agric Environ Med 22:32–34
Belluco S, Patuzzia I, Riccia A (2018) Bovine meat versus pork in Toxoplasma gondii transmission in Italy: a quantitative risk assessment model. Int J Food Microbiol 269:1–11
Burrells A, Taroda A, Opsteegh M, Schares G, Benavides J, Dam-Deisz C, Bartley PM, Chianini F, Villena I, van der Giessen J, Innes EA, Katzer F (2018) Detection and dissemination of Toxoplasma gondii in experimentally infected calves, a single test does not tell the whole story. Parasites Vectors 11:1–8
Camargo ME (1973) Introdução às técnicas de imunofluorescência. Revista Brasileira de Patologia Clínica 10:143–171
Cantos GA, Prando MD, Siqueira MV, Teixeira RM (2000) Toxoplasmose: ocorrência de anticorpos anti-Toxoplasma gondii e diagnóstico. Revista da Associação Médica Brasileira 46:335–341
Centro Panamericano de Zoonoses-CEPANZO (1973) Procedimientos para estudios de prevalencia de enfermidades crônicas enel ganado. Buenos Aires, Ramos Mejia
Cook AJ, Gilbert RE, Bufolano W, Zufferey J, Petersen E, Jenum PA, Foulon W, Semprini AE, Dunn DT (2000) Sources of Toxoplasma infection in pregnant women: European multicentre case-control study, European research network on congenital toxoplasmosis. BMJ 321:142–147
Dard C, Fricker-Hidalgo H, Brenier-Pinchart M-P, Pelloux H (2016) Relevance of and new developments in serology for toxoplasmosis. Trends Parasitol 32:492–506
Dong H, Lu YY, Su RJ, Wang YH, Wang MY, Jiang YB, Yan YR (2018) Low prevalence of antibodies against Toxoplasma gondii in dairy cattle from China’s central region. BMC Vet Res 14:1–8
Dubey JP, Hill DE, Jones JL, Hightower AW, Kirkland E, Roberts JM, Marcet PL, Lehmann T, Vianna MC, Miska K, Sreekumar C, Kwok OC, Shen SK, Gamble HR (2005) Prevalence of viable Toxoplasma gondii in beef, chicken and pork from retail meat stores in the United States: risk assessment to consumers. J Parasitol 91:1082–1093
Dubey JP, Lago EG, Gennari SM, Su C, Jones JL (2012) Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology 139:1375–1424
Dubey JP (1996) Strategies to reduce transmission of Toxoplasma gondii to animals and humans. Vet Parasitol 64:65–70
Dubey JP (1986) A review of toxoplasmosis in cattle. Vet Parasitol 22:177–202
Dubey JP (2010) Toxoplasmosis of animals and humans, 2nd edn. CRC Press, Boca Raton
Dubey JP, Jones JL (2008) Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol 38:1257–1278
Eduardo MBP, Katsuya EM, Ramos SRTS, Pavanello EI, Paiva OR, Brito SN, Madalosso G (2007) Investigação do surto de toxoplasmose associado ao consumo de prato à base de carne crua (“steak tartar”), nos municípios de São Paulo e Guarujá, SP - Novembro de 2006. Boletim Epidemiológico Paulista 4:1–4
Elfahal AM, Elhassan AM, Hussien MO, Enan KA, Musa AB, El Hussein AM (2013) Seroprevalence of Toxoplasma gondii in Dairy Cattle with reproductive problems in Sudan. ISRN Vet Sci 2013:1–4
FAO/WHO (2014) Multicriteria-based ranking for risk management of food-borne parasites. Microbiol Risk Assess Ser 23:132–140
Franco-Hernandez EN, Acosta A, Cortés-Vecino J, Gómez-Marín JE (2016) Survey for Toxoplasma gondii by PCR detection in meat for human consumption in Colombia. Parasitol Res 115:691–695
Guo M, Dubey JP, Hill D, Buchanan RL, Gamble HR, Jones JL, Pradhan AK (2015) Prevalence and risk factors for Toxoplasma gondii infection in meat animals and meat products destined for human consumption. J Food Prot 78:457–476
Hanley JA, Negassa A, Edwardes MDB, Forrester JE (2003) Statistical analysis of correlated data using generalized estimating equations: an orientation. Am J Epidemiol 157:364–375
Hosein S, Limon G, Dadios N, Guitian J, Blake DP (2016) Toxoplasma gondii detection in cattle: a slaughterhouse survey. Vet Parasitol 228:126–129
IBGE-Instituto Brasileiro de Geografia e Estatística (2012) Censo agropecuário 2006, produção de leite, availableat http://www.sidra.ibge.gov.br/bda/tabela/listabl.asp?z0t&o024&i0P&c0932. Accessed 3 Feb 2012
IBGE (2015) Instituto Brasileiro de Geografia e Estatísticas. Pesquisa Pecuária Municipal 2015. http://www.ibge.gov.br/home/estatistica/pesquisas/pesquisa_resultados.php?id_pesquisa=21. Accessed 23 Feb 2016
Jokelainen P, Tagel M, Mõtus K, Viltrop A, Lassen B (2017) Toxoplasma gondii seroprevalence in dairy and beef cattle: large-scale epidemiological study in Estonia. Vet Parasitol 236:137–143
Jones JL, Kruszon-Moran D, Wilson M, McQuillan G, Navin T, McAuley JB (2001) Toxoplasma gondii infection in the United States: seroprevalence and risk factors. Am J Epidemiol 154:357–365
Khames M, Yekkour F, Fernández-Rubio C, Aubert D, Nguewa P, Isabelle VI (2018) Serological survey of cattle toxoplasmosis in Medea, Algeria. Vet Parasitol Reg Stud Rep 12:89–90
Macedo MFSB, Macedo CAB, Barros LD, Martins GF, Sandeski LM, Zulpo DL, Da Cunha IAL, Taroda A, Cardim ST, Garcia JL (2012) Serum occurrence of anti-Toxoplasma gondii in dairy cows slaughtered in an abattoir for human consume. Ciência Rural 42:1065–1069
Marana E.R.M., Navarro I.T., Vidotto O., Freire R.L., Venturini A.C.H. 1995. Ocorrência de anticorpos anti-Toxoplasma gondii em rebanhos de bovinos de leite do Norte do Estado do Paraná-Brasil. Semina: Ciências Agrárias, 16:40–42
Marino AMF, Percipalle M, Giunta RP, Salvaggio A, Caracappa G, Alfonzetti T, Aparo A, Reale S (2017) Development and validation of a real-time PCR assay for the detection of Toxoplasma gondii DNA in animal and meat samples. J Vet Diagn Investig 29:203–207
Matsuo K, Rika K, Uetsu H, Goto H, Takashima Y, Nagamune K (2014) Seroprevalence of Toxoplasma gondii infection in cattle, horses, pigs and chickens in Japan. Parasitol Int 63:638–639
Ministério da Saúde (2007) Surto de Toxoplasmose adquirida, Anápolis-GO, fevereiro de 2006. Boletim eletrônico Epidemiológico da Secretária de Vigilância em Saúde. Brasília, vol 8, pp 1–6
Neto EC, Anele E, Rubim R, Brites A, Schulte J, Becker D, Tuuminen T (2000) High prevalence of congenital toxoplasmosis in Brazil estimated in 3-year prospective neonatal screening study. Int J Epidemiol 29:941–947
Opsteegh M, Schares G, Van der Giessen J, on behalf of the Consortium (2016) Relationship between seroprevalence in the main livestock species and presence of Toxoplasma gondii in meat (GP/EFSA/BIOHAZ/2013/01). An extensive literature review. Final report. EFSA supporting publication 2016294 (EN-996)
Opsteegh M, Teunis P, Züchner L, Koets A, Langelaar M, Giessen JVD (2011) Low predictive value of seroprevalence of Toxoplasma gondii in cattle for detection of parasite DNA. Int J Parasitol 41:343–354
Pagmadulam B, Myagmarsuren P, Fereig RM, Igarashi M, Yokoyama N, Battsetseg B, Nishikawa Y (2018) Seroprevalence of Toxoplasma gondii and Neospora caninum infections in cattle in Mongolia. Vet Parasitol Reg Stud Rep 14:11–17
Pop A, Oprisan A, Pop A, Cerbu A, Staravache M, Niyu R (1989) Toxoplasmosis prevalence parasitologically evaluated in meat animals. Archives Roumaines Pathologie Expérimentales et de Microbiologie 48:373–378
Reiczigel J, Földi J, Ózsvári L (2010) Exact confidence limits for prevalence of a disease with an imperfect diagnostic test. Epidemiol Infect 138:1674–1678
Sakikawa M, Noda S, Hanaoka M, Nakayama H, Hojo S, Kakinoki S, Nakata M, Yasuda T, Ikenoue T, Kojima T (2012) Anti-Toxoplasma antibody prevalence, primary infection rate, and risk factors in a study of toxoplasmosis in 4,466 pregnant women in Japan. Clin Vaccine Immunol 19:365–367
Sanati H, Fard SRN, Nahrevanian H, Khalili M, Safari Z (2012) Seroprevalence of Toxoplasma gondii antibodies in dairy cows in Kerman Province, South East Iran. Curr Res J Biol Sci 4:417–421
Santos TR, Costa AJ, Toniollo GH, Luvizotto MCR, Benetti AH, Santos RR et al (2009) Prevalence of anti-Toxoplasma gondii antibodies in dairy cattle, dogs, and humans from the Jauru microregion, Mato Grosso State, Brazil. Vet Parasitol 161:324–326
Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis 17:7–15
Schares G, Bangoura B, Randau F, Goroll T, Ludewig M, Maksimov P, Matzkeit B, Sens M, Bärwald A, Conraths FJ, Opsteegh M, Van der Giessen J (2017) High seroprevalence of Toxoplasma gondii and probability of detecting tissue cysts in backyard laying hens compared with hens from large free-range farms. Int J Parasitol 47:765–777
Schoonman LB, Wilsmore T, Swai ES (2010) Sero-epidemiological investigation of bovine toxoplasmosis in traditional and smallholder cattle production systems of Tanga Region, Tanzania. Trop Anim Health Prod 42:579–587
Sergeant ESG (2009) Epitools epidemiological calculators. Australian Veterinary Animal Health Services and Australian Biosecurity Cooperative Research Centre for Emerging Infectious Disease, available at: http://epitools.ausvet.com.au. Accessed 25 Jan 2018
Sharif M, Amouei A, Sarvi S, Mizani A, Mohsen AM, Hosseini S-A, Daryani A (2017) Genetic diversity of Toxoplasma gondii isolates from ruminants: a systematic review. Int J Food Microbiol 258:38–49
Shwab EK, Zhu XQ, Majumdar D, Pena HF, Gennari SM, Dubey JP, Su C (2014) Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology 141:453–461
Simon JA, Kurdzielewicz S, Jeanniot E, Dupuis E, Marnef F, Aubert D, Villena I, Poulle ML (2017) Spatial distribution of soil contaminated with Toxoplasma gondii oocysts in relation to the distribution and use of domestic cat defecation sites on dairy farms. Int J Parasitol 47:357–367
Souza AM, Pereira RA, Yokoo EM, Levy RB, Sichieri R (2013) Alimentos mais consumidos no Brasil: Inquérito Nacional de Alimentação 2008-2009. Revista de Saúde Pública 47:190S–199S
Spagnol FH, Paranhos EB, Oliveira LLS, Medeiros SM, Lopes CWG, Albuquerque GR (2009) Prevalência de anticorpos anti-Toxoplasma gondii em bovinos abatidos em matadouros do estado da Bahia, Brasil. Revista Brasileira Parasitologia Veterinária 18:42–45
Stelzer S, Basso W, Benavides SJ, Ortega-Mora LM, Maksimov P, Gethmann J, Conraths FJ, Schares G (2019) Toxoplasma gondii infection and toxoplasmosis in farm animals: risk factors and economic impact. Food Waterborne Parasitol 15:1–101
Sun W-W, Meng Q-F, Cong F, Shan X-F, Wang C-F, Qian A-D (2015) Herd-level prevalence and associated risk factors for Toxoplasma gondii, Neospora caninum, Chlamydia abortus and bovine viral diarrhoea virus in commercial dairy and beef cattle in eastern, northern and northeastern China. Parasitol Res 114:4211–4218
Tan QD, Yang XY, Yin MY, Hu LY, Qin SY, Wang JL, Zhou DH, Zhu XQ (2015) Seroprevalence and correlates of Toxoplasma gondii infection in dairy cattle in northwest China. Acta Parasitologica 60:618–621
Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii: from animals to humans. Int J Parasitol 30:1217–1258
Yildiz K, Kul O, Babur C, Kilic S, Gazyagci AN, Celebi B, Gurcan IS (2009) Seroprevalence of Neospora caninum in dairy cattle ranches with high abortion rate: special emphasis to serologic co-existence with Toxoplasma gondii, Brucella abortus and Listeria monocytogenes. Vet Parasitol 164:306–310
Acknowledgements
We thank the FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais), for financial support (CBB APQ-00855/13).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Guimarães, A.M., Bruhn, F.R.P., da Rocha, C.M.B.M. et al. Seroepidemiology of Toxoplasma gondii in Dairy Cows in Southeastern Brazil: Seropositive Cows on All Farms Investigated. Acta Parasit. 65, 628–635 (2020). https://doi.org/10.2478/s11686-019-00140-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11686-019-00140-x