Seroprevalence and risk factors for Toxoplasma gondii infection in pigs in southern Piauí

Soroprevalência e fatores de risco para infecção por Toxoplasma gondii em suínos no Sul do Piauí

Richard Átila de Sousa Jezlon da Fonseca Lemos Leonardo Atta Farias Carla Duque Lopes Karina Rodrigues dos Santos About the authors

Abstracts

This study is aimed to assess the prevalence and risk factors associated with T. gondii infection in pigs. We evaluated 143 pigs, in 10 randomly-chosen farms located in Southern Piauí. The pig's blood serum was analyzed through ELISA in detection of anti-T. gondii antibodies. A seroprevalence of 25.5% was observed in the pigs that reacted against T. gondii antigens. The data from the records demonstrated an association with some factors such as: age, diet, type of management, breed and presence of cats in the farms with a prevalence of T. gondii. With the exception of sex, all others features represent risk factors for T. gondii infection. Furthermore, our data contributed to the understanding of the T. gondiiseroprevalence in pig farms located in Southern Piauí.

Toxoplasmosis; pig; seroprevalence; Piauí


Este estudo teve como objetivo avaliar a soroprevalência e os fatores de risco associados a infecção por T. gondiiem suínos. Foram avaliados 143 suínos em 10 propriedades localizadas no Sul do Estado do Piauí. Os soros dos suínos foram analisados para a detecção de anticorpos anti-T. gondii pela técnica de ELISA. Encontrou-se uma soroprevalência de 25,5% em suínos reativos para antígenos de T. gondii. Por meio de fichas, alguns fatores como idade, dieta, raça, sistema de criação e presença de gatos foram associados à presença de T. gondii. Com exceção do sexo, todas as outras características representaram fatores de risco para a infecção com o parasita. Os dados contribuem para a compreensão da soroprevalência de T. gondii de suínos criados no Sul do Estado do Piauí.

Toxoplasmose; suínos; soroprevalência; Piauí


T. gondii is the toxoplasmosis agent, a disease that is usually benign in immunocompetent individuals; however it can be severe or fatal in children with congenital diseases or in immunosupressed patients (DUBEY et al., 2012Dubey JP, Lago EG, Gennari SM, SU C, Jones JL. Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology 2012; 139(11): 1375-1424. http://dx.doi.org/10.1017/S0031182012000765
http://dx.doi.org/10.1017/S0031182012000...
). In farmed animals, such as sheep, pigs and goats, infection by T. gondii is common and can lead to great economic loss through stillbirths, miscarriages and birth defects (UZÊDA et al., 2004Uzêda RS, Fernández SY, Jesus EEV, Pinheiro AM, Ayres MCC, Spinola S, et al. Fatores relacionados à presença de anticorpos IgG anti-Toxoplasma gondii em caprinos leiteiros do Estado da Bahia. Rev Bras Saúde Prod An 2004; 5(1): 1-8.). Food-borne transmission of T. gondii is considered to be the most important route for human infection (PEREIRA et al., 2010Pereira KS, Franco RM, Leal DA. Transmission of toxoplasmosis (Toxoplasma gondii) by foods. Adv Food Nutr Res 2010; 60: 1-19. http://dx.doi.org/10.1016/S1043-4526(10)60001-0
http://dx.doi.org/10.1016/S1043-4526(10)...
; DAVIES, 2011Davies PR. Intensive Swine Production and Pork Safety Foodborne. Pathog Dis 2011; 8(2):189-201. http://dx.doi.org/10.1089/fpd.2010.0717
http://dx.doi.org/10.1089/fpd.2010.0717...
), which occurs through the ingestion of tissue cysts while handling or eating raw or undercooked meat. Free-range meat production is a trend that may increase the risk of parasite-infection. Most importantly, the consumption of raw or undercooked meat from T. gondiiinfected pigs represents the major risk for T. gondii infection in humans (DUBEY, 2009Dubey JP. Toxoplasmosis in pigs – The last 20 years. Vet Parasitol 2009; 164(2-4): 89-103. http://dx.doi.org/10.1016/j.vetpar.2009.05.018
http://dx.doi.org/10.1016/j.vetpar.2009....
; DUBEY et al., 2012Dubey JP, Lago EG, Gennari SM, SU C, Jones JL. Toxoplasmosis in humans and animals in Brazil: high prevalence, high burden of disease, and epidemiology. Parasitology 2012; 139(11): 1375-1424. http://dx.doi.org/10.1017/S0031182012000765
http://dx.doi.org/10.1017/S0031182012000...
). According to the Associação Brasileira de Indústria Produtora e Exportação de Carne Suína – ABIPECS (2011), Brazil exported over 582 thousand tons, of swine meat, in 2011. The State of Piauí holds 17% of the swine herd in the northeast region and represents the third largest herd in northeastern Brazil (IBGE, 2006). Despite the importance of pork supply in Brazil, no study of T. gondii prevalence has been carried out in this region. Hence, this study is the first one to correlate T. gondii seroprevalence and possible risk factors for T. gondii infection and transmission among swine herds in the southern region of the State of Piauí.

In order to conduct this study, one hundred and forty-three samples were randomly collected from 10 swine farms located in six of the eleven cities of the Alto-Médio Gurguéia region, in the south of Piauí (Table 1), throughout the months of November and December 2010. This study was approved by the Comitê de Ética em Experimentação com Animais – CEEA/UFPI (n°. 060/2010). At the time the samples were collected, some of the animal's characteristics were registered in individual sheets, including location, number and age, conditions of confinement (intensive or semi-intensive production), food and water offered and presence or not of cats in the farms (Table 2). Blood samples were collected and the seraum obtained was used to detect IgG antibodies against T. gondii by ELISA, as described by Silva et al., (1997)Silva DAO, Cabral DD, Bernardina BLD, Souza MA, Mineo JR. Detection of Toxoplasma gondii-specific antibodies in dogs. A comparative study of immunoenzymatic, immunofluorescent and haemagglutination titers. Mem Inst Oswaldo Cruz 1997; 92(6): 785-789. http://dx.doi.org/10.1590/S0074-02761997000600010
http://dx.doi.org/10.1590/S0074-02761997...
. The samples' results were seropositive when ELISA Index (EI) > 1.2. Statistical analysis was performed using the GraphPad Prism 4.0 software (Graphpad Sofware Inc., San Diego, USA). Seropositivity percentages were compared through the Chi-square (χ2) test or Fisher exact test, when appropriate. Values of P < 0.05 were considered statistically significant.

Table 1.
Distribution of seropositive or seronegative pig samples for T. gondii. Analysis of the cities located in the Alto Medio Gurguéia region, during the months of November and December, 2010.

Table 2.
Description of environmental and farm management and pig characteristics and co-related with anti-Toxoplasma gondii antibodies in pigs from Southern Piauí.

According to the results, 25.5% (37) of the samples collected presented antibodies to T. gondii. Despite the high prevalence, our results are similar to those found in pigs in other Brazilian States: 17,22% in Santa Catarina (PERDONCINI et al., 2010Perdoncini G, Pasquali AKS, Mariani F, Cembranel DJ, Escopelli KS. Prevalência de Toxoplasma gondii em aves e suínos: um problema para a saúde pública. UNOESC e Ciência – ACBS 2010; 1(1): 57-64.); 25.5% in Paraná (MILLAR et al., 2008Millar PR, Daguer H, Vicente RT, Costa T, Sobreiro LG, Amendoeira MRR. Toxoplasma gondii: estudo soro-epidemiológico de suínos da região sudoeste do estado do Paraná. Pesq Vet Bras 2008; 28(1): 15-18. http://dx.doi.org/10.1590/S0100-736X2008000100002
http://dx.doi.org/10.1590/S0100-736X2008...
) and 50% in Belém (FREITAS et al., 2009Freitas JA, Oliveira JP, Ramos OS, Ishizuka MM. Frequência de anticorpos anti-Toxoplasma gondii em suínos abatidos sem inspeção em Belém. Arqo Bras Med Vet Zootec 2009; 61(5): 1230-1232. http://dx.doi.org/10.1590/S0102-09352009000500030
http://dx.doi.org/10.1590/S0102-09352009...
). Animals tested positive for T. gondii were detected in all the analyzed cities. Among all the regions Cristino Castro, presented the highest number of seropositives pigs, followed by the cities of Bom Jesus and Currais (Table 1). Considering all the studied characteristics, only variables such as sex and reason for rearing (animals designated to subsistence agriculture or to industrial manipulation) were not considered as risk factors for infection by T. gondii (Table 2). A recent review reported that the association between sex and T. gondii seroconvertion is a bias linked to the high number of females in the studies collected (DA SILVA et al., 2010Da Silva AV, Silva RC, Zamprogna TO, Lucas TM. Toxoplasma gondii em suínos com ênfase na contribuição brasileira. Sci Med 2010; 20(1): 120-130.). We obtained a balanced number of females and males (ratio of 1.47) and, therefore, the data from this study in southern Piauí refutes the relationship between sex and T. gondii infection in pigs, and supports the data collected by Frazão-Teixeira and Oliveira (2011)Frazão-Teixeira E, Oliveira FCR. Anti–Toxoplasma gondii antibodies in cattle and pigs in a highly endemic area for human toxoplasmosis in Brazil. J Parasitoo 2011; 97(1): 44-47. http://dx.doi.org/10.1645/GE-2457.1
http://dx.doi.org/10.1645/GE-2457.1...
. Another recognized risk factor for infection by T. gondii in livestock is the pig's age (DA SILVA et al., 2008). Our data also demonstrated that exposure to parasites increased with the animal's age (χ2 = 10.12, p = 0.00015). The final pig's phase was found to be the most susceptible to T. gondii (41%) (Table 2). Additionally, the pigs in the culling state presented a higher level of T. gondii antibodies compared to the piglets. According to Da Silva et al. (2010)Da Silva AV, Silva RC, Zamprogna TO, Lucas TM. Toxoplasma gondii em suínos com ênfase na contribuição brasileira. Sci Med 2010; 20(1): 120-130., the pig's age is closely associated to the risk of infection in humans, as the older pig's carcasses are generally used in the preparation of swine products. The type of food supply-used also offers risks of contamination. Pigs fed with human food scraps presented more antibodies to T. gondii (100%), compared to pigs that received ration (16.6%) and those fed on both diets (χ2 = 41.05, p < 0.0001) (Table 2). These particular results showed the precarious situation of swine farming in southern Piauí, where herds are still fed with human food scraps, probably, favoring the life cycle of T. gondii. Accordingly, our results indicate that the swine reared in an intensive system were less exposed to T. gondii(18.5%) than those maintained in a semi-intensive system (48.5%) (χ2 = 12.45, p < 0.0004) (Table 2). The risk of the semi-intensive method is associated with the animal's access to soil or water contaminated with parasite oocysts (SUARÉZ-ARANDA et al., 2000Suaréz-Aranda F, Galisteo AJ, Hiramoto RM, Cardoso RP, Meireles LR, Miguel O, et al. The prevalence and avidity of Toxoplasma gondii IgG antibodies in pigs from Brazil and Peru. Vet Parasitol 2000; 91(1-2): 23-32. http://dx.doi.org/10.1016/S0304-4017(00)00249-1
http://dx.doi.org/10.1016/S0304-4017(00)...
). The pig's exposure to both risk factors: semi-intensive system and human food feeding, probably justified the high exposure of T. gondii among the non defined breed pig (χ2 = 41.36, p < 0.0001). Another important risk factor for T. gondii infection was the presence of cats in the farms (29.9%) (χ2 = 15.74, p< 0.0001) (Table 2). The presence of cats increases T. gondii seroconvertion in pigs by 2.6 fold (ASSADI-RAD et al., 1995Assadi-Rad AM, New JC, Patton S. Risk factors associated with transmission of Toxoplasma gondii to sows kept in different management systems in Tenessee. Vet Parasitol 1995; 57(4): 289-297. http://dx.doi.org/10.1016/0304-4017(94)00677-5
http://dx.doi.org/10.1016/0304-4017(94)0...
) mainly depositing the oocysts form into the soil or water and, therefore; creating high environmental contamination (ORTEGA-PACHECO et al., 2011Ortega-Pacheco A, Acosta-Viana KY, Guzman-Marin E, Uitzil-Álvarez B, Rodríguez-Buenfil JC, Jimenez-Coello M. Infection dynamics of Toxoplasma gondii, in two fattening pig farms exposed to high and low cat density in an endemic region. Vet Parasitol 2011; 175(3-4):367-371. http://dx.doi.org/10.1016/j.vetpar.2010.10.018
http://dx.doi.org/10.1016/j.vetpar.2010....
). It can be concluded that the data obtained in this study is a warning of the risks of local T. gondii infection and transmission to the human population.

We thank Dr. Maria Cristina Roque-Barreira for laboratorial and material support.

References

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  • Assadi-Rad AM, New JC, Patton S. Risk factors associated with transmission of Toxoplasma gondii to sows kept in different management systems in Tenessee. Vet Parasitol 1995; 57(4): 289-297. http://dx.doi.org/10.1016/0304-4017(94)00677-5
    » http://dx.doi.org/10.1016/0304-4017(94)00677-5
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    » http://dx.doi.org/10.1089/fpd.2010.0717
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    » http://dx.doi.org/10.1016/j.vetpar.2009.05.018
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    » http://dx.doi.org/10.1017/S0031182012000765
  • Frazão-Teixeira E, Oliveira FCR. Anti–Toxoplasma gondii antibodies in cattle and pigs in a highly endemic area for human toxoplasmosis in Brazil. J Parasitoo 2011; 97(1): 44-47. http://dx.doi.org/10.1645/GE-2457.1
    » http://dx.doi.org/10.1645/GE-2457.1
  • Freitas JA, Oliveira JP, Ramos OS, Ishizuka MM. Frequência de anticorpos anti-Toxoplasma gondii em suínos abatidos sem inspeção em Belém. Arqo Bras Med Vet Zootec 2009; 61(5): 1230-1232. http://dx.doi.org/10.1590/S0102-09352009000500030
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    » http://dx.doi.org/10.1590/S0100-736X2008000100002
  • Ortega-Pacheco A, Acosta-Viana KY, Guzman-Marin E, Uitzil-Álvarez B, Rodríguez-Buenfil JC, Jimenez-Coello M. Infection dynamics of Toxoplasma gondii, in two fattening pig farms exposed to high and low cat density in an endemic region. Vet Parasitol 2011; 175(3-4):367-371. http://dx.doi.org/10.1016/j.vetpar.2010.10.018
    » http://dx.doi.org/10.1016/j.vetpar.2010.10.018
  • Perdoncini G, Pasquali AKS, Mariani F, Cembranel DJ, Escopelli KS. Prevalência de Toxoplasma gondii em aves e suínos: um problema para a saúde pública. UNOESC e Ciência – ACBS 2010; 1(1): 57-64.
  • Pereira KS, Franco RM, Leal DA. Transmission of toxoplasmosis (Toxoplasma gondii) by foods. Adv Food Nutr Res 2010; 60: 1-19. http://dx.doi.org/10.1016/S1043-4526(10)60001-0
    » http://dx.doi.org/10.1016/S1043-4526(10)60001-0
  • Silva DAO, Cabral DD, Bernardina BLD, Souza MA, Mineo JR. Detection of Toxoplasma gondii-specific antibodies in dogs. A comparative study of immunoenzymatic, immunofluorescent and haemagglutination titers. Mem Inst Oswaldo Cruz 1997; 92(6): 785-789. http://dx.doi.org/10.1590/S0074-02761997000600010
    » http://dx.doi.org/10.1590/S0074-02761997000600010
  • Suaréz-Aranda F, Galisteo AJ, Hiramoto RM, Cardoso RP, Meireles LR, Miguel O, et al. The prevalence and avidity of Toxoplasma gondii IgG antibodies in pigs from Brazil and Peru. Vet Parasitol 2000; 91(1-2): 23-32. http://dx.doi.org/10.1016/S0304-4017(00)00249-1
    » http://dx.doi.org/10.1016/S0304-4017(00)00249-1
  • Uzêda RS, Fernández SY, Jesus EEV, Pinheiro AM, Ayres MCC, Spinola S, et al. Fatores relacionados à presença de anticorpos IgG anti-Toxoplasma gondii em caprinos leiteiros do Estado da Bahia. Rev Bras Saúde Prod An 2004; 5(1): 1-8.

Publication Dates

  • Publication in this collection
    Jan-Mar 2014

History

  • Received
    27 June 2013
  • Accepted
    29 Jan 2014
Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
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