INTRODUCTION
The Taenia saginata-cysticercosis is a disease caused by one parasite that requires two hosts during its life cycle. Human beings and bovines are considered as definitive and intermediate hosts, respectively. The cattle infections occur through the ingestion of T. saginata eggs (Lopes et al. Reference Lopes, Cruz, Soares, Nunes, Teixeira, Maciel, Buzulini, Pereira, Felippelli, Thomaz-Soccol, Oliveira and Costa2014).
Bovine cysticercosis is the most common disease detected during inspection of cattle's carcasses and viscera in Brazil. The prevalence values are probably underestimated because the ongoing model of sanitary inspection has a low sensitivity due to the possible presence of cysticerci in muscles and viscera, which are not routinely inspected (Lopes et al. Reference Lopes, Santos, Soares, Nunes, Mendonça, Lima, Sakamoto, Costa, Thomaz-Soccol, Oliveira and Costa2011.). However, meat inspection is required in order to avoid its transmission to human beings and to provide information for health institutions regarding its occurrence in farms, municipalities and regions (Onyango-Abuje et al. Reference Onyango-Abuje, Hughes, Opicha, Nginyi, Wright and Harrison1996; Minozzo et al. Reference Minozzo, Gusso, Castro, Lago and Soccol2002; Fukuda, Reference Fukuda2003; Giovannini et al. Reference Giovannini, Carvalho, Cabral, Brasil and Santos2014).
The states of Goiás, Mato Grosso, Mato Grosso do Sul, São Paulo, Minas Gerais, Pará and Rondônia raised 72% of bovines, which were slaughtered in Brazil, contributing to keep the country in the second position in the raking of world's beef producers and allowing export of beef to 143 countries. Additional values of 1·9 and 4·4% in beef production and export in Brazil is estimated from 2014 through 2024 (BRASIL, 2014).
There is a need of developing and adopting sanitary control programmes during cattle raising in Brazil in order to reduce the risk of T. saginata-cysticercosis transmission worldwide considering the raising tendency of Brazilian beef export. According to Brazil (1952), carcasses considered as infected need to be heat-treated using freezing in order to inactivate the parasite.
To neglect this disease causes trade barriers and estoppels to Brazilian beef in global market and also economical losses to beef production chain (Rossi et al. Reference Rossi, Hoppe, Mathias, Martins, Mussi and Prata2015).
The prevalence of bovine cysticercosis in Brazil is 1·05% and differences on its value is reported among several states. In Goiás, the reported prevalence is 0·78% (Dutra et al. Reference Dutra, Girotto, Vieira, Vieira, Zangirolamo, Marquês, Headley and Vidotto2012).
In order to contribute to the knowledge about bovine cysticercosis epidemiology in this state, this study aimed to assess the prevalence and spatial distribution of bovine cysticercosis in the state of Goiás, Brazil; to verify its association with epidemiological variables, and to establish the economical losses for beef farms.
MATERIALS AND METHODS
A retrospective study regarding bovine cysticercosis occurrence was performed through accessing the database from Brazilian Ministry of Agriculture, Livestock and Food Supply (MAPA http://www.agricultura.gov.br/assuntos/inspecao/produtos-animal/sif/servico-de-inspecao-federal-sif), which contains data provided by the Federal Inspection Service (SIF). A set of 23 255 979 bovines from 246 municipalities in the state of Goiás, Brazil, including both genders and age ranging from 18 to 60 months were inspected through the years 2007–2014.
The animals were slaughtered according to the standardized technology, and the carcasses and viscera were inspected according to Brazilian legislation (Brazil, 1952). SIF adopts post-mortem inspection for bovine cysticercosis through incisions in muscles (masseteres, pterygoids, tongue and heart), palpation and visual examination of head, viscera and carcasses external surfaces according to the Regulation of Sanitary and Industrial Inspection of Animal's Products Origin (RIISPOA) (Brazil, 1952). The cysticerci were classified as viable and unviable according to their characteristics (translucent or opaque, respectively).
The obtained data were grouped per year (from 2007 to 2014), mesoregions and microregions from this state (Figures 1AB). This study included five mesoregions (Central, East, North, Northeast and South) and 18 microregions (Anápolis, Anicuns, Aragarças, Catalão, Ceres, Chapada dos Veadeiros, Entorno do Distrito Federal, Goiânia, Iporá, Meia Ponte, Pires do Rio, Porangatu, Quirinópolis, Rio Vermelho, São Miguel do Araguaia, Sudoeste de Goiás, Vale do Rio dos Bois and Vão do Paranã) according to the classification from Brazilian Institute of Geography and Statistics (IBGE, 2016, http://cidades.ibge.gov.br/xtras/uf.php?lang=&coduf=52&search=goias).
Fig. 1. Mesoregions (a) and microregions (b) in the state of Goiás, Brazil.
The prevalence and the 95% confidence interval (95% CI) were calculated through the Wilson's method (Thrusfield, Reference Thrusfield2010). The relation among bovine cysticercosis in municipalities, mesoregions and microregions was calculated using that one with the lower prevalence [considered as odds ratio (OR) = 1] and the others were compared with it. Z test was used to evaluate significance (P < 0·05) (Thrusfield, Reference Thrusfield2010).
Data regarding the human population density (inhab per km2), Human Development Index (IDH), poverty incidence index, cattle population size, area of temporary tillage (ha), grassland area (ha), sugarcane area (ha), farmer condition (seated without definitive title) and numbers of houses without sanitary room were obtained from IBGE website (http://cidades.ibge.gov.br/xtras/uf.php?lang=&coduf=52&search=goias). The classification of tourism practices was also obtained through from the state of Goiás Government website (www.goiasturismo.go.gov.br).
The association among bovine cysticercosis prevalence in municipalities (dichotomized using the median value – zero and one for the values below and above, respectively) with epidemiological factors, such as human population density (inhab/km2), forage area (ha), sugar cane area (ha), producer's condition (settled with or without permanent title), houses without sanitary room and touristic practices.
A simple binary logistic regression analysis was applied to all variables mentioned above, and those with P ≤ 0·20 were selected.
Then, a multivariate binary logistic regression analysis was performed using the significant variables in the univariate analysis (P ≤ 0·20). The strength of the association between dependent and independent variables was estimated by OR, which was obtained from logistic regression estimations (P ≤ 0·05).
The economic losses were estimated based on bovine cysticercosis prevalence and the penalties applied to farms suppliers of infected cattle using the scheme adopted by slaughterhouses in this state. Carcasses with intense cysticercosis infections, i.e. more than one cysticercus in an area of about 22 cm2, must be rendered and consequently the producer is not paid. Mild-to-moderate infections require freezing or canning and the producer receives 30–50% of the value, for unviable or viable cysticercosis, respectively. The carcasses’ weight were considered as 225 kg and their value was gathered from Center of Advanced Studies and Applied Economy – ESALQ/USP (CEPEA) from December from 2017 to 2014. The dollar conversion rate used was |US$1·00 = R$3·15 (reais).
Statistical analyses were performed using software Epi Info, v. 7.1.5.2 (https://www.cdc.gov/epiinfo/index.html). Maps were created using the Terraview® software (http://www.dpi.inpe.br/terraview/index.php_) through quantile method (divided in four categories).
RESULTS
A set of 123 728 bovines were considered as infected with cysticerci from the 23 255 979 animals slaughtered (prevalence = 0·53; 95% CI 0·5295–0·5354) through the years 2007–2014 in the state of Goiás, Brazil. Among the cysticerci detected, 52 351 and 71 377 were considered as viable and unviable, respectively. The areas considered with high-bovine cysticercosis prevalence (viable and unviable) are located in the centre of the state of Goiás (Figs. 2A and B).
Fig. 2. Spatial distribution of bovine cysticercosis prevalence in the state of Goiás, Brazil, through the years 2007–2014. (a) viable cysticerci; (b) unviable cysticerci.
The Central mesoregion was considered as the one with the highest prevalence (P = 1·01%; 95% CI 4·2936–4·5895) during this period, while South (0·62%), North (0·23%) and Northeast (0·23%) regions showed low-prevalence values (Figs. 2A and B and Table 1).
Table 1. Analysis of association between the mesoregions of the state of Goiás, referring to the prevalence of bovine cysticercosis diagnosed between 2007 and 2014
Mesoregions with OR >1 and CI 95% >1 had higher risk for bovine cysticercosis occurrence.
A significant statistical difference (P ≤ 0·05 on risk for bovine cysticercosis occurrence through the years was observed at 2008 (OR = 1·31; CI 1·2650–1·3664), 2013 (OR = 1·07; CI 1·0271–1·1170) and 2014 (OR = 1·34; CI 1·2884–1·3958). However, the areas considered as with higher prevalence were not modified (Fig. 3 and Table 2).
Fig. 3. Spatial distribution of bovine cysticercosis prevalence in municipalities in the state of Goiás, Brazil, through the years 2007–2014.
None of the variables, such as human population density (inhab per km2), IDH, poverty incidence index, cattle population size, area of temporary tillage (ha), grassland area (ha), sugarcane area (ha), farmer condition (seated without definitive title), numbers of residences without sanitary room and municipalities categorized as touristic, were significantly associated (P > 0·05) with bovine cysticercosis prevalence in municipalities.
This study performed a simulation of the economic losses during the study period using the prevalence value in this state (0·53%), carcasses weight (225 kg) and carcasses prices (Table 3). The economical losses for beef farmers located in the state of Goiás ranged from US$9 260 728·57 to US$11 313 816·67 due to the presence of unviable and viable cysticercosis, respectively, without considering the economical losses that occur due to beef rendering (100% of discount on paid value).
Table 2. Analysis of association between the microregions of the state of Goiás, referring to the prevalence of bovine cysticercosis diagnosed between 2007 and 2014
Microregions with OR >1 and CI 95% >1 had higher risk for bovine cysticercosis occurrence.
Table 3. Losses (simulation discount of 30–50% off) generated to the rural producers in the state of Goiás by the occurrence of cysticercosis (calcified and alive), from 2007 to 2014
a Mean body weight of each animal estimated at 15 arrobas (@); total weigh in @ = N. cases * 15@.
b Market value for the month of December of the corresponding year – CEPEA, Center for Advanced Studies in Applied Economics – ESALQ/USP http://www.cepea.esalq.usp.br.
c Exchange rate: US$1·00 = R$3·15.
DISCUSSION
No significant association (P > 0·05) was found in this study between bovine cysticercosis prevalence in municipalities and epidemiological variables, such as human population density per km2, HDI, poverty incidence index, cattle population size, area of temporary tillage (ha), grassland area (ha), sugarcane area (ha), farmer condition (seated without definitive title), numbers of residences without sanitary room and municipalities categorized as touristic. The absence of statistical correlation probably occurred due the low variability of values of bovine cysticercosis prevalence in municipalities located in the state of Goiás (ranged from 0·15 to 0·50%) (Table 3) or a homogeneity of the other variable values.
The prevalence value assessed in this study (0·53%; 95% CI 0·5295–0·5354) was higher than that reported by Santos and Moreira (Reference Santos and Moreira2010) in the state of Minas Gerais, Brazil (0·37%). This difference probably occurred due to differences on data obtaining. These authors used viable cysticerci counting to establish prevalence value, while in our study, the prevalence was 0·23% using the same criteria.
This value (0·53%) was lower than others obtained in several studies (using the same criteria), as those performed by Dutra et al. (Reference Dutra, Girotto, Vieira, Vieira, Zangirolamo, Marquês, Headley and Vidotto2012); Silva et al. (Reference Silva, Rocha, Oliveira and Netto2012) and Rossi et al. (Reference Rossi, Hoppe, Mathias, Martins, Mussi and Prata2015). These authors established values of bovine cysticercosis prevalence of 0·78, 3·23 and 0·71%, respectively. It is important to emphasize that these results refers to data obtained in the same state, but these differences are difficult to explain due to differences on the criteria used in other studies, such as sample size and the period.
The prevalence value assessed in this study (0·53%) is lower than the value reported in Brazil (1·05%) (Dutra et al. Reference Dutra, Girotto, Vieira, Vieira, Zangirolamo, Marquês, Headley and Vidotto2012), and in the states of Paraná (2·2%) (Guimarães-Peixoto et al. Reference Guimarães-Peixoto, Souza, Pinto and Santos2012) and São Paulo (4·8%) (Ferreira et al. Reference Ferreira, Revoredo, Ragazzi, Soares, Ferraldo, Mendonça and Lopes2014). In the other hand, the prevalence is similar to the value reported in the state of Mato Grosso (0·08%) (Rossi et al. Reference Rossi, Simoni, Lopes, Almeida, Soares, Vidal, Ferraudo and Mathias2016), which is located in the same Brazilian region (West-Centre). A possible explanation for this difference of bovine cysticercosis prevalence among the states of Paraná/São Paulo and Mato Grosso/Goiás is the differences on human population density (pop. per km2). The values in the states of Paraná and São Paulo are 52·4 and 166·2, while it is 3·3 and 17·6 in Mato Grosso and Goiás, respectively. The differences on population size of definitive and intermediate hosts influence T. saginata life cycle and bovine cysticercosis prevalence (Rossi et al. Reference Rossi, Simoni, Lopes, Almeida, Soares, Vidal, Ferraudo and Mathias2016).
A similarity can be observed comparing the prevalence assessed in this study with those reported in other countries, such as Iran (0·25%) (Khaniki et al. Reference Khaniki, Raei, Kia, Haghi and Selseleh2010), Chile (0·58%) (Faustina et al. Reference Faustina, Gaston, Enrique, Veronica, Willy and Carmen2012) and European countries (<1%) (Laranjo-González et al. Reference Laranjo-González, Devleesschauwer, Gabriel, Dorny and Allepuz2016).
The no-detection of bovine cysticercosis in animals slaughtered from two municipalities does not mean a real absence of this disease at these areas due to the low sensitivity of the ongoing model of meat inspection and the practice of slaughter without inspection (illegal), which remains occurring in this state (Lopes et al. Reference Lopes, Santos, Soares, Nunes, Mendonça, Lima, Sakamoto, Costa, Thomaz-Soccol, Oliveira and Costa2011).
Another important result is the similarity observed in the municipalities in the state of Goiás regarding the prevalence of animals infected with viable and unviable cysticercosis. There is an ideology that the risk for T. saginata-cysticercosis occurrence need to be assessed using data of viable cysticerci detection due to animal's movement in several farms during their raising, not allowing to establish in which farm the infection occurred. However, it is important to mention that the areas with higher prevalence of viable and unviable cysticercosis were very similar for evaluation in municipalities (Figs. 2A and B).
Ferreira et al. (Reference Ferreira, Revoredo, Ragazzi, Soares, Ferraldo, Mendonça and Lopes2014) stated that bovine cysticercosis is not only related to bovine population size but also is closely related to the presence of human beings. The comparison among bovine cysticercosis prevalence (viable and unviable) with cattle distribution in this state is shown in Figs. 4A and B. Besides that, in this study, similarity or tendency between prevalence of bovine cysticercosis and high human population is observed in their spatial distribution as shown in Figs. 4A and C.
Fig. 4. Spatial distribution of bovine cysticercosis prevalence (a), cattle population size (b) and human population density (c) in municipalities in the state of Goiás, Brazil, through the years 2007–2014.
Besides the low value of bovine cysticercosis prevalence in the state of Goiás compared with other Brazilian states, this disease causes important economical losses for beef farms and cattle slaughterhouses. Thus, sanitary programmes aiming its control need to be adopted in Brazil. These programmes need to include prophylactic measures useful to control the risk factors reported in Brazil, such as the access to contaminated water or raising of animals in high-populated areas (Ferreira et al. Reference Ferreira, Revoredo, Ragazzi, Soares, Ferraldo, Mendonça and Lopes2014; Rossi et al. Reference Rossi, Hoppe, Mathias, Martins, Mussi and Prata2015; Rossi et al. Reference Rossi, Simoni, Lopes, Almeida, Soares, Vidal, Ferraudo and Mathias2016).
The economical losses due to bovine cysticercosis occurrence in this Brazilian state through 8 years ranged from US$9 260 728·57 to US$11 313 816·67 without considering the economical losses due to rendering of infected carcasses. Furthermore, according to the data published in Annual Report 2015, the Brazilian beef production chain in Brazil generated R$380 billion during 2013 and sale of cattle to slaughter generated R$62·7 billion (BRAZIL, 2014). Comparing these values with the economical losses during 2013 (R$12 million) due to the occurrence of only one disease (bovine cysticercosis) in one low-prevalent Brazilian state (Goiás), allow us to infer that the economical losses are really important for Brazilian beef production chain considering the high prevalence of this disease in other Brazilian states.
Concluding remarks
Bovine cysticercosis prevalence in the state of Goiás, Brazil, was 0·53% (95% CI 0·5295–0·5354) from 2007 to 2014. The mesoregions (Central and South) and the microregions Goiânia, Anápolis, Pires do Rio and Vale do Rio dos Bois showed a higher risk for bovine cysticercosis detection. The economical losses ranged from US$9 260 728·57 to 11 313 816·67 due to occurrence of unviable and viable cysticercosis, respectively. These results highlight the importance of meat inspection to improve the knowledge about high-occurrence areas that requires interventions in order to reduce the economical losses for beef production chain.
FINANCIAL SUPPORT
This research received no specific grant from any funding agency, commercial or not-for-profit sectors.
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