Toxoplasma gondii and Neospora caninum infections and factors associated in goats in the Parana state, Southern Brazil

Infecções por Toxoplasma gondii e Neospora caninum e fatores associados em caprinos no estado do Paraná, Sul do Brasil

Paulo Roberto Romanelli Andressa Maria Rorato Nascimento de Matos Fernanda Pinto-Ferreira Eloiza Teles Caldart Juliana Silva de Oliveira Gabriela Anteveli Brenda Caroline dos Santos Jeanfelice Rafael Luiz Stolf Tainá Favoreto Sanches Mariana Kassab e Silva Alessandro Pelegrine Minho Antônio Cezar Rocha Cavalcante Roberta Lemos Freire Regina Mitsuka-Breganó Italmar Teodorico Navarro About the authors

Abstract

The aim of this study was to determine the occurrence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies and their associated factors among goats in farms from the Paraná state, South Brazil. The serological analysis was performed by indirect ELISA on 629 goat serum samples collected from 32 farms distributed in five mesorregions from the state. Seropositivity was observed in 30.7% of the animals for T. gondii, 6.3% for N. caninum, and 3.0% for both agents. Final multiple regression models showed that the use of assisted reproduction decreased the chance of seropositivity for T. gondii (PR=0.70) and the slaughtering site on the farm (PR=2.03) increased it. To N. caninum, the supplying concentrated feed to animals (OR=4.80) and animal pre-weaning death (OR=9.96) increased the chance of seropositivity. The variables associated with these seropositivities suggest deficiencies in sanitation and reproductive management. In addition, it recognizes critical points of infection for animal production management.

Keywords:
Seroprevalence; Toxoplasma gondii; Neospora caninum; goats; Brazil

Resumo

O objetivo desse estudo foi avaliar a ocorrência de anticorpos anti-Toxoplasma gondii e anti-Neospora caninum e seus fatores associados em caprinos de propriedades do Estado do Paraná, Sul do Brasil. A análise sorológica foi realizada, utilizando-se ELISA indireto em 629 amostras de soro caprino, coletadas em 32 propriedades distribuídas em cinco mesorregiões do Estado. A soropositividade foi observada em 30,7% dos animais para T. gondii, 6,3% para N. caninum e 3,0% para ambos. Os modelos finais de regressão múltipla mostraram que o uso de reprodução assistida reduziu a chance de soropositividade para T. gondii (PR=0,70), enquanto a presença no local de abate na fazenda (PR=2,03) aumentou. Para N. caninum, o fornecimento de ração concentrada (OR=4,80) e a morte dos animais no pré-desmame (OR=9,96) aumentaram a chance de soropositividade. O estudo das variáveis associadas às soropositividades sugere deficiências no saneamento e no manejo reprodutivo dos Animais. Além disso, reconhece pontos críticos para a infecção no manejo da produção animal.

Palavras-chave:
Soroprevalência; Toxoplasma gondii; Neospora caninum; caprinos; Brasil

Introduction

The national goat herd was estimated at 9,614,722 million heads (IBGE, 2014Instituto Brasileiro de Geografia e Estatística – IBGE. Estatísticas do registro civil [online]. Rio de Janeiro: IBGE; 2014 [cited 2019 Nov 14]. Available from: https://biblioteca.ibge.gov.br/visualizacao/periodicos/135/rc_2014_v41.pdf
https://biblioteca.ibge.gov.br/visualiza...
). According to the register of herds of the Secretariat of Agriculture and Supply, Paraná accounts for 1.6% of the national goat population, ranking eighth in the nation, with approximately 115,718 thousand heads (Paraná, 2019Paraná. Governo do Estado. Secretaria de Estado da Agricultura e do Abastecimento – SEAB. Departamento de Economia Rural – DERAL. Números da Pecuária Paranaense - Ano 2019 [online]. Curitiba: SEAB; 2019 [cited 2020 July 28]. Available from: http://www.agricultura.pr.gov.br/system/files/publico/Conjuntura/nppr.pdf
http://www.agricultura.pr.gov.br/system/...
), demonstrating the importance of goat farming in the state. Among the diseases that affect goats is the toxoplasmosis, caused by Toxoplasma gondii, which is one of the main agents responsible for reproductive dysfunction. The prevalence of T. gondii in Brazil is quite variable, with reported prevalence rates of 14.4% in São Paulo (Mainardi et al., 2003Mainardi RS, Modolo JR, Stachissini AVM, Padovani CR, Langoni H. Soroprevalência de Toxoplasma gondii em rebanhos caprinos no Estado de São Paulo. Rev Soc Bras Med Trop 2003; 36(6): 759-761. http://dx.doi.org/10.1590/S0037-86822003000600021. PMid:15049121.
http://dx.doi.org/10.1590/S0037-86822003...
), 17.1% in Rio Grande do Norte (Lima et al., 2008Lima JTR, Ahid SMM, Barrêto RA Jr, Pena HFJ, Dias RA, Gennari SM. Prevalence to Toxoplasma gondii and Neospora caninum antibodies in goats from Mossoró, Rio Grande do Norte. Braz J Vet Res Anim Sci 2008; 45(2): 81-86. http://dx.doi.org/10.11606/issn.1678-4456.bjvras.2008.26703.
http://dx.doi.org/10.11606/issn.1678-445...
), 49.4% in Piauí (Rêgo et al., 2016Rêgo WMF, Paula NRO, Vitor RWA, Silva RAB, Diniz BLM, Sousa M, et al. Risk factors for Toxoplasma gondii infection in goats and sheep raised in the State of Piauí in northeast Brazil. Small Rumin Res 2016; 141: 17-23. http://dx.doi.org/10.1016/j.smallrumres.2016.04.010.
http://dx.doi.org/10.1016/j.smallrumres....
), and 39.4% in Paraná (Garcia et al., 2012Garcia G, Sotomaior C, Nascimento AJ, Navarro IT, Soccol VT. Toxoplasma gondii in goats from Curitiba, Paraná, Brazil: risks factors and epidemiology. Rev Bras Parasitol Vet 2012; 21(1): 42-47. http://dx.doi.org/10.1590/S1984-29612012000100009. PMid:22534944.
http://dx.doi.org/10.1590/S1984-29612012...
). In addition, to the direct damage caused by T. gondii, such as miscarriages and stillbirths, they can be major sources of infection to humans, through the consumption of raw or under cooked meat, raw milk, and its by-products (Dubey et al., 2014Dubey JP, Verma SK, Ferreira LR, Oliveira S, Cassinelli AB, Ying Y, et al. Detection and survival of Toxoplasma gondii in milk and cheese from experimentally infected goats. J Food Prot 2014; 77(10): 1747-1753. http://dx.doi.org/10.4315/0362-028X.JFP-14-167. PMid:25285492.
http://dx.doi.org/10.4315/0362-028X.JFP-...
).

Another parasite that can cause reproductive problems is Neospora caninum, first described in 2004 by Figliuolo et al. (2004)Figliuolo LPC, Rodrigues AAR, Viana RB, Aguiar DM, Kasai N, Gennari SM. Prevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in goat from São Paulo State, Brazil. Small Rumin Res 2004; 55(1–3): 29-32. http://dx.doi.org/10.1016/j.smallrumres.2003.12.013.
http://dx.doi.org/10.1016/j.smallrumres....
that reported the prevalence of 6.4% in goat herds in the state of São Paulo. Since then, several studies have been conducted in other states such Paraíba (3.3%; Faria et al., 2007Faria EB, Gennari SM, Pena HFJ, Athayde ACR, Silva MLCR, Azevedo SS. Prevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in goats slaughtered in the public slaughterhouse of Patos city, Paraíba State, Northeast region of Brazil. Vet Parasitol 2007; 149(1–2): 126-129. http://dx.doi.org/10.1016/j.vetpar.2007.07.009. PMid:17706359.
http://dx.doi.org/10.1016/j.vetpar.2007....
; and 26.11%; Braz et al., 2018Braz BMA, Valente JDM, Villalobos EMC, Lara MCCSH, Machado CAL, Barbosa IC, et al. Seroepidemiology of Neospora caninum among goats (Capra hircus) in the state of Paraíba, northeastern Brazil. Arq Bras Med Vet Zootec 2018; 70(1): 147-152. http://dx.doi.org/10.1590/1678-4162-9453.
http://dx.doi.org/10.1590/1678-4162-9453...
), Rio Grande do Norte (1.05%; Lima et al., 2008Lima JTR, Ahid SMM, Barrêto RA Jr, Pena HFJ, Dias RA, Gennari SM. Prevalence to Toxoplasma gondii and Neospora caninum antibodies in goats from Mossoró, Rio Grande do Norte. Braz J Vet Res Anim Sci 2008; 45(2): 81-86. http://dx.doi.org/10.11606/issn.1678-4456.bjvras.2008.26703.
http://dx.doi.org/10.11606/issn.1678-445...
), and Pernambuco (64,2%; Tembue et al., 2011Tembue AA, Ramos RA, Sousa TR, Albuquerque AR, Costa AJ, Meunier IM, et al. Serological survey of Neospora caninum in small ruminants from Pernambuco State, Brazil. Rev Bras Parasitol Vet 2011; 20(3): 246-248. http://dx.doi.org/10.1590/S1984-29612011000300013. PMid:21961757.
http://dx.doi.org/10.1590/S1984-29612011...
; and 2.04%; Arraes-Santos et al., 2016Arraes-Santos AI, Araújo AC, Guimarães MF, Santos JR, Pena HFJ, Gennari SM, et al. Seroprevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in domestic mammals from two distinct regions in the semi-arid region of Northeastern Brazil. Vet Parasitol Reg Stud Rep 2016; 5: 14-18. http://dx.doi.org/10.1016/j.vprsr.2016.08.007. PMid:31014531.
http://dx.doi.org/10.1016/j.vprsr.2016.0...
). Although the various serologic studies in Brazilian goats’ herds, the reproductive impairment caused by N. caninum is still scarce evaluated (Braz et al., 2018Braz BMA, Valente JDM, Villalobos EMC, Lara MCCSH, Machado CAL, Barbosa IC, et al. Seroepidemiology of Neospora caninum among goats (Capra hircus) in the state of Paraíba, northeastern Brazil. Arq Bras Med Vet Zootec 2018; 70(1): 147-152. http://dx.doi.org/10.1590/1678-4162-9453.
http://dx.doi.org/10.1590/1678-4162-9453...
).

Toxoplasmosis and neosporosis represent important reproductive and economic losses in the country's goat herds (Dubey, 2010Dubey JP. Toxoplasmosis of animals and humans. 2nd ed. Florida: CRC-Press; 2010.; Dubey et al., 2017Dubey JP, Hemphill A, Calero-Bernal R, Schares G. Neosporosis in animals. Florida: CRC-Press; 2017. http://dx.doi.org/10.1201/9781315152561.
http://dx.doi.org/10.1201/9781315152561...
). In addition, these diseases have an important role in public health, since this herds can be a source of T. gondii infection for men (Dubey & Beattie, 1988Dubey JP, Beattie CP. Toxoplasmosis of animals and man. Florida: CRC-Press; 1988.; Mesquita et al., 2013Mesquita LP, Nogueira CI, Costa RC, Orlando DR, Bruhn FR, Lopes PF, et al. Antibody kinetics in goats and conceptuses naturally infected with Neospora caninum. Vet Parasitol 2013; 196(3-4): 327-333. http://dx.doi.org/10.1016/j.vetpar.2013.03.002. PMid:23537945.
http://dx.doi.org/10.1016/j.vetpar.2013....
). Thus, the identification of factors associated with infection is essential to support programs for the development and promotion of goat farming worldwide (Topazio et al., 2014Topazio JP, Weber A, Camillo G, Vogel FF, Machado G, Ribeiro A, et al. Seroprevalence and risk factors for Neospora caninum in goats in Santa Catarina state, Brazil. Rev Bras Parasitol Vet 2014; 23(3): 360-366. http://dx.doi.org/10.1590/S1984-29612014062. PMid:25271457.
http://dx.doi.org/10.1590/S1984-29612014...
). The present study aimed to evaluate the seropositivity of T. gondii and N. caninum and the factors associated with their positivity in Paraná state, Brazil.

Materials and Methods

The study was approved by the Ethics Committee for Animal Use - EMBRAPA Goats and Sheep, Sobral - CE (number 010/2014). These activities were part of the project EMBRAPA (Zoosanitary characterization of goat and sheep farming in Brazil: epidemiology, associated factors and economic impact of diseases, number 02.12.01.032.00). To calculate the sample size (n), an infinite population was used as a reference using EpiInfo 7.2.3.1. The estimated prevalence were based on the study by Fortes et al. (2017)Fortes MS, Lopes-Mori FMR, Caldart ET, Constantino C, Evers F, Pagliari S, et al. Caprine toxoplasmosis in Southern Brazil: a comparative seroepidemiological study between the indirect immunofluorescence assay, enzyme-linked immunosorbent assay, and the modified agglutination test. Trop Anim Health Prod 2017; 50(2): 413-419. http://dx.doi.org/10.1007/s11250-017-1450-1. PMid:29079943.
http://dx.doi.org/10.1007/s11250-017-145...
, in which T. gondii was estimated to have a prevalence of 33.3%, and an error of 4%, resulting in a sample size of 533 animals, and the study by Figliuolo et al. (2004)Figliuolo LPC, Rodrigues AAR, Viana RB, Aguiar DM, Kasai N, Gennari SM. Prevalence of anti-Toxoplasma gondii and anti-Neospora caninum antibodies in goat from São Paulo State, Brazil. Small Rumin Res 2004; 55(1–3): 29-32. http://dx.doi.org/10.1016/j.smallrumres.2003.12.013.
http://dx.doi.org/10.1016/j.smallrumres....
, who estimated a prevalence of 6.4% and an error of 2% for N. caninum, resulting in a sample size of 575 animals.

A non-probabilistic sampling was carried out to choose the farms because of a lack of a list of all goat producers in the state of Paraná. Farms were chosen in the municipalities with the greatest representation in goat farming from the mesoregions: Central North, Metropolitan of Curitiba, West, Southwest and Center-South. Within each farm, the animals used were stratified according to age (approximately 60% of adult females, 35% from 6 to 12 months old animals, and all adult males

The blood was sampled by jugular puncture in a tube without anticoagulant and kept refrigerated until the centrifugation for obtaining the serum. The detection of anti-T gondii IgG antibodies was performed by an indirect ELISA technique as described by Garcia et al. (2007)Garcia JL, Navarro IT, Biazzono L, Freire RL, Guimarães JS Jr, Cryssafidis AL, et al. Protective activity against oocyst shedding in cats vaccinated with crude rhoptry proteins of the Toxoplasma gondii by the intranasal route. Vet Parasitol 2007; 145(3-4): 197-206. http://dx.doi.org/10.1016/j.vetpar.2007.01.007. PMid:17296268.
http://dx.doi.org/10.1016/j.vetpar.2007....
. The standardized T. gondii antigen concentration was 2.5 μg mL-1, the sera were titrated at a ratio of 1:100 and the conjugate (Sigma Aldrich®, USA) was diluted to a ratio of 1:4,000. All the samples were tested in duplicate. The optimal conditions concerning antigen concentration, serum titration and conjugate dilution were established by the highest ratio of mean absorbance of positive samples to mean absorbance of negative samples. The cutoff point for each plate was obtained according to Garcia et al. (2006)Garcia JL, Navarro IT, Vidotto O, Gennari SM, Machado RZ, Luz Pereira AB, et al. Toxoplasma gondii: comparison of a rhoptry-ELISA with IFAT and MAT for antibody detection in sera of experimentally infected pigs. Exp Parasitol 2006; 113(2): 100-105. http://dx.doi.org/10.1016/j.exppara.2005.12.011. PMid:16458299.
http://dx.doi.org/10.1016/j.exppara.2005...
using the mean negative sera plus three standard deviations. For the detection of anti-N. caninum antibodies, commercial indirect Elisa kits (Imunodot®, Jaboticabal, Brazil) were used. The cutoff index (CFI) was calculated by multiplying the mean optical density of the negative controls by 2.5; the positive samples exhibited a bright yellow color and had an optical density equal to or greater than the CFI, as described by the manufacturer.

A questionnaire was applied to each property with information such as: infrastructure, characteristics of production and commercialization, technological profile, sanitation and presence of other species on the property, domestic and wild. Of each animal whose blood was collected, sex, age and breed information were obtained. The EpiInfo 7.2.3.1 program was used to tabulate the variables from the epidemiological questionnaire along with the serological results and for bivariate analysis. The variables from the epidemiological questionnaire were screened by Yates-corrected chi-square (χ2) and Fisher's exact tests, and those with P <0.20 were selected for inclusion in the regression analysis. The existence of associated factors was estimated by multiple logistic regression or multiple log-binomial regression, and the strength of the association was estimated by odds ratio (OR) or prevalence ratio (PR) and their respective 95% confidence intervals using R environment 3.6.2 version, packages epitools (Aragon, 2020Aragon TJ. Epitools: Epidemiology Tools. R package version 0.5-10.1 [online]. 2020 [cited 2020 May 5]. Available from: https://CRAN.R-project.org/package=epitools
https://CRAN.R-project.org/package=epito...
) and epiDisplay (Chongsuvivatwong, 2018Chongsuvivatwong V. epiDisplay: Epidemiological Data Display Package. R package version 3.5.0.1 [online]. 2018 [cited 2020 May 5]. Available from: https://CRAN.R-project.org/package=epiDisplay
https://CRAN.R-project.org/package=epiDi...
).

Results and Discussion

This study included 19 municipalities from five of the ten mesoregions in the state of Paraná, and 629 animals from 32 farms were evaluated. The distribution of the agents on the farms indicated that 90.6% (29/32) of the farms were positive for T. gondii and 53.1% (17/32) were positive for N. caninum, demonstrating an important distribution of agents on farms in Paraná (Table 1). Frequencies of 6.3% for anti-Neospora caninum IgG antibodies (39/629; 95% CI = 4.6-8.4) and 30.7% for anti-Toxoplasma gondii IgG antibodies (193/629; 95% CI = 27.2 - 34.4) were found in the studied goat population (Table 1). The frequency of antibodies to both agents was 3.0% (19/629). To date, no prevalence studies on N. caninum have been performed in goats in the state of Paraná. However, Fortes et al. (2017)Fortes MS, Lopes-Mori FMR, Caldart ET, Constantino C, Evers F, Pagliari S, et al. Caprine toxoplasmosis in Southern Brazil: a comparative seroepidemiological study between the indirect immunofluorescence assay, enzyme-linked immunosorbent assay, and the modified agglutination test. Trop Anim Health Prod 2017; 50(2): 413-419. http://dx.doi.org/10.1007/s11250-017-1450-1. PMid:29079943.
http://dx.doi.org/10.1007/s11250-017-145...
described a 33.3% (352/1058) prevalence of T. gondii in the state of Paraná, like our study positivity (193/629; 95% CI = 27.2-34.4); both studies used iELISA as the diagnosis method.

Table 1
Frequency of anti-Toxoplasma gondii and anti-Neospora caninum antibodies by mesoregion in goat farms of Paraná state, Brazil.

The bivariate data analysis revealed an association between the T. gondii positivity and the following variables: use of assisted reproduction methods on the farm, the presence of cats on the farm, the presence of wild felines on the farm, the presence of animals who drink water directly from the source, the existence of a slaughtering site on the farm, supplying placental remains to cats, supplying concentrated feed to animals, and the presence of animals over eight months (Table 2). In the final multiple regression model, the following variables were adjusted for: the use of assisted reproduction methods on the farm (P = 0.0042; PR = 0.70, 95% CI = 0.55-0.89) and the existence of a slaughtering site on the farm (P <0.0001; PR = 2.03, 95% CI = 1.59-2.60) (Table 3).

Table 2
Frequencies and bivariate analysis (P<0.20) from variables statistically associated with the positivity of anti-Toxoplasma gondii antibodies in goats from Paraná state, Brazil.
Table 3
Final models of multiple regression analysis from variables statistically associated with the positivity of anti-Toxoplasma gondii antibodies in goats from Paraná state, Brazil, (P<0.05).

The assisted reproduction variable (controlled breeding and artificial insemination), compared to uncontrolled natural breeding, was a protective factor for the positivity of T. gondii in the present study. Pereira et al. (2012)Pereira MF, Peixoto RM, Langoni H, Greca H Jr, Azevedo SS, Porto WJN, et al. Fatores de risco associados à infecção por Toxoplasma gondii em ovinos e caprinos no estado de Pernambuco. Pesq Vet Bras 2012; 32(2): 140-146. http://dx.doi.org/10.1590/S0100-736X2012000200009.
http://dx.doi.org/10.1590/S0100-736X2012...
found a significant association for natural breeding, which increased the chance of toxoplasmosis occurrence by 6.09, in the multivariate analysis. Farms in which assisted reproductive techniques are used may represent the adoption of good production practices and management and improved selection of breeders, indicating proper sanitary care as well as beneficial management techniques. In addition, it was not a significant association between reproductive impairment and toxoplasmosis and/or neosporosis. Similar results are observed with N. caninum prevalence in goats of Paraíba state (Braz et al., 2018Braz BMA, Valente JDM, Villalobos EMC, Lara MCCSH, Machado CAL, Barbosa IC, et al. Seroepidemiology of Neospora caninum among goats (Capra hircus) in the state of Paraíba, northeastern Brazil. Arq Bras Med Vet Zootec 2018; 70(1): 147-152. http://dx.doi.org/10.1590/1678-4162-9453.
http://dx.doi.org/10.1590/1678-4162-9453...
); however, it was contrary with other studies about T. gondii.

The slaughter of animals on rural farms, even if transported to a specific site for this purpose, does not always occur under satisfactory hygienic-sanitary conditions. In addition, blood and viscera may collect on the floor, which is highly attractive to cats. The presence of rodents in supplement stores is another condition that is attractive to cats that end up defecating and eliminating oocysts that are later ingested by the livestock via food (Romanelli et al., 2007Romanelli PR, Freire RL, Vidotto O, Marana ER, Ogawa L, De Paula VS, et al. Prevalence of Neospora caninum and Toxoplasma gondii in sheep and dogs from Guarapuava farms, Paraná State, Brazil. Res Vet Sci 2007; 82(2): 202-207. http://dx.doi.org/10.1016/j.rvsc.2006.04.001. PMid:17266999.
http://dx.doi.org/10.1016/j.rvsc.2006.04...
). Weigel et al. (1999)Weigel RM, Siegel AM, Dyer D, Dubey JP. Risk factors for infection with Toxoplasma gondii for residents and workers on swine farms in Illinois. Am J Trop Med Hyg 1999; 60(5): 793-798. http://dx.doi.org/10.4269/ajtmh.1999.60.793. PMid:10344655.
http://dx.doi.org/10.4269/ajtmh.1999.60....
suggested that the presence of cats on rural farms is the main risk factor for environmental contamination and human infection by T. gondii. Cavalcante et al. (2008)Cavalcante ACR, Carneiro M, Gouveia AMG, Pinheiro RR, Vitor RWA. Risk factors for infection by Toxoplasma gondii in herds of goats in Ceará, Brazil. Arq Bras Med Vet Zootec 2008; 60(1): 36-41. http://dx.doi.org/10.1590/S0102-09352008000100006.
http://dx.doi.org/10.1590/S0102-09352008...
reported that the risk of T. gondii infection in goat was increased by 1.73 times in farms from Ceará state with more than 10 cats This finding is explained by the free breeding of these animals which had access to various zootechnical facilities, pastures and natural water supply and storage sources. Although wild felids do not inhabit the human peridomiciliary, they have free access to pastures, where they often feed on animal carcasses and placental remains, become infected and subsequently spread T. gondii oocysts throughout the environment through their feces.

Regarding age, a significant association was observed for animals older than eight months, which increased the chance of toxoplasmosis by 2.53 times. Anderlini et al. (2011)Anderlini GA, Mota RA, Faria EB, Cavalcanti EFTSF, Valença RMB, Pinheiro Júnior JW, et al. Occurrence and risk factors associated with infection by Toxoplasma gondii in goats in the State of Alagoas, Brazil. Rev Soc Bras Med Trop 2011; 44(2): 157-162. http://dx.doi.org/10.1590/S0037-86822011005000017. PMid:21503550.
http://dx.doi.org/10.1590/S0037-86822011...
found a positive association for the prevalence of T. gondii in adult animals compared to younger goats in herds from Alagoas state. Jittapalapong et al. (2005)Jittapalapong S, Sangvaranond A, Pinyopanuwat N, Chimnoi W, Khachaeram W, Koizumi S, et al. Seroprevalence of Toxoplasma gondii infection in domestic goats in Satun Province, Thailand. Vet Parasitol 2005; 127(1): 17-22. http://dx.doi.org/10.1016/j.vetpar.2004.08.019. PMid:15619370.
http://dx.doi.org/10.1016/j.vetpar.2004....
observed that older animals (older than two years) were 2.70 times more likely to be T. gondii-seropositive. This is explained by the fact that there is an increased chance of animals becoming infected over time due to oocyst ingestion from the contaminated environment.

In relation to water source, Cavalcante et al. (2008)Cavalcante ACR, Carneiro M, Gouveia AMG, Pinheiro RR, Vitor RWA. Risk factors for infection by Toxoplasma gondii in herds of goats in Ceará, Brazil. Arq Bras Med Vet Zootec 2008; 60(1): 36-41. http://dx.doi.org/10.1590/S0102-09352008000100006.
http://dx.doi.org/10.1590/S0102-09352008...
found that contamination was associated with the poor sanitation of drinking fountains and facilities used for capturing and storing large volumes of water, which are practically impossible to sanitize, thus becoming sources of infection to animals. This result was corroborated by Villari et al. (2009)Villari S, Vesco G, Petersen E, Crispo A, Buffolano W. Risk factors for toxoplasmosis in pigs bred in Sicily, Southern Italy. Vet Parasitol 2009; 161(1-2): 1-8. http://dx.doi.org/10.1016/j.vetpar.2009.01.019. PMid:19246158.
http://dx.doi.org/10.1016/j.vetpar.2009....
, who described a correlation between untreated water supplied to animals and the presence of anti-T. gondii antibodies. The epidemiological analysis results of water contamination by T. gondii oocysts can be extrapolated to water contamination by N. caninum oocysts from dog feces. The implementation of good hygiene practices on the farms is essential to avoid environmental contamination of food and water by T. gondii and N. caninum oocysts (Machacova et al., 2015Machacova T, Bartova E, Sedlak K, Budikova M, Piccirillo A. Risk factors involved in transmission of Toxoplasma gondii and Neospora caninum infection in rabbit farms in Northern Italy. Ann Agric Environ Med 2015; 22(4): 677-679. http://dx.doi.org/10.5604/12321966.1185774. PMid:26706976.
http://dx.doi.org/10.5604/12321966.11857...
).

The variables supplying concentrated feed to animals and animal pre-weaning death were factors associated with the positivity of neosporosis in goats in Paraná state according to the bivariate analysis (Table 4). In the final multiple logistic regression model, two variables were associated factors, supplying concentrated feed to animals, which increased the odds of N. caninum seropositivity by 4.80 times (P = 0.0356; 95% CI = 1.32-74.70), and animal pre-weaning death, which increased the odds by 9.96 times (P = 0.0253; 95% CI = 1.11-20.75) (Table 5). Table 5 shows that the odds ratio confidence intervals calculated by the logistic regression method are wide, and this maybe is due to the small number of seropositive animals for N. caninum. Feed supplementation with concentrates is a necessary practice in ruminant animal breeding during grazing shortages. However, the storage of this food product requires appropriate conditions. Although the presence of dogs was not a significant variable in this study, dogs are commonly found sheltering in these places, where they end up defecating, eliminating N. caninum oocysts in the feces and contaminating stored food, as described by Dubey & Schares (2011)Dubey JP, Schares G. Neosporosis in animals – the last five years. Vet Parasitol 2011; 180(1-2): 90-108. http://dx.doi.org/10.1016/j.vetpar.2011.05.031. PMid:21704458.
http://dx.doi.org/10.1016/j.vetpar.2011....
. In the present study, a mortality rate of 8.6% pre-weaning period was observed, but no etiological diagnosis was made. The observation of neonatal deaths or miscarriages may not be a direct result of neosporosis; however, there is a likelihood of spread among herds when dogs eventually feed on placental or miscarriage material or the remains of neonates who were infected with N. caninum during pregnancy. However, Buxton et al. (2002)Buxton D, McAllister MM, Dubey JP. The comparative pathogenesis of neosporosis. Trends Parasitol 2002; 18(12): 546-552. http://dx.doi.org/10.1016/S1471-4922(02)02414-5. PMid:12482540.
http://dx.doi.org/10.1016/S1471-4922(02)...
reported that the first infection of N. caninum in sheep and goats can be fatal to the fetus; however, in subsequent pregnancies, fetal infection may be relatively uncommon, a fact attributed to maternal immunity in these species.

Table 4
Frequencies and bivariate analysis (P<0.20) from variables statistically associated with the positivity of anti-Neospora caninum antibodies in goats from Paraná state, Brazil.
Table 5
Final models of multiple regression analysis from variables statistically associated with the positivity of anti-Neospora caninum antibodies in goats from Paraná state, Brazil, (P<0.05).

Conclusion

This research highlights the positivity for anti-T. gondii and anti-N. caninum antibodies in goats in the state of Paraná. The variables associated with these seropositivity suggest deficiencies in sanitation and reproductive management; such as presence of cats, that feed on placental remains, the lack of a suitable place for slaughter on the farm, to drink water straight from the source, the occurrence of pre-weaning death and do not to use assisted reproduction methods. In addition, recognizes critical points of infection for the animal production management, like to provide concentrated feed, do not avoid the presence of wild felids on the farm and to have animals with age over eight months.

  • How to cite: Romanelli PR, Matos AMRN, Pinto-Ferreira F, Caldart ET, Oliveira JS, Anteveli G, et al. Toxoplasma gondii and Neospora caninum infections and factors associated in goats in the Parana state, Southern Brazil. Braz J Vet Parasitol 2020; 29(4): e003620. https://doi.org/10.1590/S1984-29612020076

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Publication Dates

  • Publication in this collection
    09 Oct 2020
  • Date of issue
    2020

History

  • Received
    20 Feb 2020
  • Accepted
    27 July 2020
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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