ABSTRACT:

This study determined the frequency of positive tests for bovine tuberculosis in animals and breeders/establishments in Rio Grande do Norte, Brazil. Data were provided by the Instituto de Defesa e Inspeção Agropecuária do Rio Grande do Norte (IDIARN), from its Unidade Local de Sanidade Animal e Vegetal (ULSAV’S), acquired in monthly reports issued by qualified Veterinarians under the National Program for the Control and Eradication of Brucellosis and Animal Tuberculosis (PNCEBT), from June 2012 to December 2021. For diagnosis, the comparative cervical test was used as a routine and confirmatory test. A total of 45,804 cattle were tested, 53 (0.1%) of which tested positive. Secondary data are essential in the evaluation of sanitary measures, allowing rapid generation of hypotheses about diseases and providing support for decision-making. Measures such as raising awareness among producers, sanitary control in the acquisition and sale of cows for reproduction, inspection of sanitary barriers, and conducting epidemiological surveys to understand the actual situation of this disease in the state of Rio Grande do Norte are crucial.

Key words:
Mycobacterium bovis; tuberculosis; epidemiology; frequency

RESUMO:

O objetivo do trabalho foi determinar a frequência de animais e estabelecimentos positivos para a tuberculose bovina no estado do Rio Grande do Norte, Brasil. Os dados foram fornecidos pelo Instituto de Defesa e Inspeção Agropecuária do Rio Grande do Norte (IDIARN) e são oriundos de suas Unidades Locais de Sanidade Animal e Vegetal (ULSAV) coletados dos relatórios mensais emitidos por Médicos Veterinários habilitados para atuação no âmbito do Programa Nacional de Controle e Erradicação da Brucelose e da Tuberculose Animal (PNCEBT), compreendendo o período de junho de 2012 a dezembro de 2021. Para o diagnóstico foi utilizado o Teste Cervical Comparativo (TCC) como teste de rotina e confirmatório. No total, foram testados 45.804 bovinos, dos quais 53 animais (0,1%) apresentaram resultado positivo. Os dados secundários são informações de extrema importância na avaliação de medidas sanitárias, permitindo uma rápida geração de hipóteses sobre as enfermidades e dando suporte na tomada de decisões. É fundamental a condução de medidas que incluam a conscientização dos produtores, controle sanitário na aquisição e venda de matrizes, fiscalização nas barreiras sanitárias e a realização de um inquérito epidemiológico para se conhecer a real situação desta doença no estado do Rio Grande do Norte.

Palavras-chave:
Mycobacterium bovis; tuberculose; epidemiologia; frequência

INTRODUCTION

The economy of the state of Rio Grande do Norte (RN) is based on agriculture, livestock, industry, tourism, and services. In this context, cattle farming plays an important role because it contributes to the creation of jobs and the generation of income. However, cattle farming activity still has some limitations. Poor technical skills of producers, consecutive years of drought, and infectious diseases have caused significant damage to breeders in this state (SECRETARIA DE ESTADO DO PLANEJAMENTO E DAS FINANCIAS - SEPLAN, 2016SECRETARIA DE ESTADO DO PLANEJAMENTO E DAS FINANCIAS (SEPLAN), 2016a. Diagnóstico e Planejamento Estratégico para o Desenvolvimento de Atividades Produtivas Agrícolas do Rio Grande do Norte. Available from: <Available from: http://www.rnsustentavel.rn.gov.br. >. Accessed: Aug. 13, 2018.
http://www.rnsustentavel.rn.gov.br.... ). In this regard, infectious disease, such as bovine tuberculosis caused by Mycobacterium bovis, was detected. The microorganism is adapted to cattle as its host; however, it also causes diseases in other animal species, including humans (CEZAR et al., 2016CEZAR, R. D. DA S. et al. Molecular detection of Mycobacterium bovis in cattle herds of the state of Pernambuco, Brazil. BMC Veterinary Research, v.12, n.1, p.4-9, 2016. Available from: <Available from: https://doi.org/10.1186/s12917-016-0656-1 >. Accessed: Mar. 20, 2019. doi: 10.1186/s12917-016-0656-1.
https://doi.org/10.1186/s12917-016-0656-... ). This disease has a significant economic impact, reducing meat and milk production and preventing the use of carcasses and affected parts that become unsafe for human consumption (FAO, OMS, OIE, 2017FAO; OMS; OIE. Hoja de ruta contra la tuberculosis zoonótica. 2017, Available from: <Available from: http://www.who.int/iris/handle/10665/259231 >. Accessed: Aug. 09, 2018.
http://www.who.int/iris/handle/10665/259... ).

In Brazil, the National Program for the Control and Eradication of Brucellosis and Animal Tuberculosis (PNCEBT), established in 2001 and recently updated by Normative Instruction no. 10/2017, aims to reduce the prevalence and incidence of brucellosis and tuberculosis in bovines and buffaloes by eradicating both diseases through a set of mandatory sanitary measures associated with voluntary adherence actions (BRASIL, 2017BRASIL. Instrução Normativa SDA n°10, de 3 de Março de 2017. Ministério da Agricultura, Pecuária e Abastecimento. Secretaria de Defesa Animal, 2017. Accessed: Ago. 13, 2018.). This regulation recommends the sanitary slaughter of cattle that were tested positive in the tuberculin skin test (antemortem diagnosis) and the inspection of carcasses with macroscopic lesions in abattoirs (postmortem diagnosis) (ARAÚJO et al., 2014ARAÚJO, C. P. et al. Detection of Mycobacterium bovis in bovine and bubaline tissues using nested-PCR for TbD1. PLoS ONE, v.9, n.3, p.6, 2014. Available from: <Available from: https://doi.org/10.1371/journal.pone.0091023 >. Accessed: Mar. 20, 2019. doi: 10.1371/journal.pone.0091023.
https://doi.org/10.1371/journal.pone.009... ).

Several surveys with animal-level prevalence rates of 0.0009-1.6% were conducted to characterize the epidemiological situation of bovine tuberculosis in the Federative Units of Brazil (BAHIENSE et al., 2016BAHIENSE, L. et al. Prevalence and risk factors for bovine tuberculosis in the State of Bahia, Brazil. Semina: Ciências Agrárias, v.37, n.5Supl2, p.35-49, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3549 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3549.
https://doi.org/10.5433/1679-0359.2016v3... ; BELCHIOR et al., 2016BELCHIOR, A. P. C. et al. Prevalence and risk factors for bovine tuberculosis in Minas Gerais State, Brazil. Tropical Animal Health and Production, v.48, n.2, p.373-378, 2016. Available from: <Available from: https://doi.org/10.1007/s11250-015-0961-x >. Accessed: Mar. 20, 2019. doi: 10.1007/s11250-015-0961-x.
https://doi.org/10.1007/s11250-015-0961-... ; DIAS et al., 2016DIAS, R. A. et al. Prevalence and risk factors for bovine tuberculosis in the state of São Paulo, Brazil. Semina: Ciências Agrárias, v.37, n.5, p.3673-3684, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3673 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3673.
https://doi.org/10.5433/1679-0359.2016v3... ; FERREIRA NETO et al., 2021FERREIRA NETO, J. S. et al. Situação Epidemiológica da tuberculose bovina no estado do Tocantins, Brasil. Semina: Ciências Agrárias, v.42, n.3, p.1673-1684, 2021. Available from: <Available from: https://doi.org/10.5433/1679-0359.2021v42n3Supl1p1673 >. Accessed: Jun. 03, 2023. doi: 10.5433/1679-0359.2021v42n3Supl1p1673.
https://doi.org/10.5433/1679-0359.2021v4... ; GALVIS et al., 2016GALVIS, J. O. A. et al. Epidemiologic characterization of bovine tuberculosis in the State of Espírito Santo, Brazil. Semina: Ciências Agrárias, v.37, n.5Supl2, p.3567, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3567 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3567.
https://doi.org/10.5433/1679-0359.2016v3... ; GUEDES et al., 2016GUEDES, I. B. et al. Prevalence and risk factors for bovine tuberculosis in the State of Mato Grosso do Sul, Brazil. Semina: Ciências Agrárias, v.37, n.5Supl2, p.3579, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3579 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3579.
https://doi.org/10.5433/1679-0359.2016v3... ; LIMA et al., 2016LIMA, P. R. B. et al. Epidemiological situation of bovine tuberculosis in the State of Pernambuco, Brazil. Semina: Ciências Agrárias, v.37, n.5, p.3601-3611, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3601 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3601.
https://doi.org/10.5433/1679-0359.2016v3... ; NÉSPOLI et al., 2016NÉSPOLI, J. M. B. et al. Epidemiological situation of bovine tuberculosis in the state of Mato Grosso, Brazil. Semina: Ciências Agrárias, v.37, n.5, p.3589-3600, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3601 >. Accessed: Mar. 20, 2019. doi: 10.1679-0359/2016v37n5Supl2p3589.
https://doi.org/10.5433/1679-0359.2016v3... ; QUEIROZ et al., 2016QUEIROZ, M. R. et al. Epidemiological status of bovine tuberculosis in the state of Rio Grande do Sul, Brazil. Semina: Ciências Agrárias, v.37, n.5, p.3647-3658, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3647 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3647.
https://doi.org/10.5433/1679-0359.2016v3... ; RIBEIRO et al., 2016RIBEIRO, L. A. et al. Epidemiological status of bovine tuberculosis in the Federal District of Brazil. Semina: Ciências Agrárias, v.37, n.5, p.3561-3566, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3561 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3561.
https://doi.org/10.5433/1679-0359.2016v3... ; ROCHA et al., 2016ROCHA, W. V. et al. Prevalence and herd-level risk factors of bovine tuberculosis in the State of Goiás, Brazil. Semina: Ciências Agrárias, v.37, n.5, p.3625-3638, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3625 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3625.
https://doi.org/10.5433/1679-0359.2016v3... ; SILVA et al., 2016SILVA, M. D. C. P. et al. Prevalence and herd-level risk factors for bovine tuberculosis in the State of Paraná, Brazil. Semina: Ciências Agrárias, v.37, n.5, p.3611-3624, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3611 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3611.
https://doi.org/10.5433/1679-0359.2016v3... ; VELOSO et al., 2016VELOSO, F. P. et al. Prevalence and herd-level risk factors of bovine tuberculosis in the State of Santa Catarina. Semina: Ciências Agrárias, v.37, n.5, p.3659-3672, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3659 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3659.
https://doi.org/10.5433/1679-0359.2016v3... ; VENDRAME et al., 2016VENDRAME, F. B. et al. Epidemiologic characterization of bovine tuberculosis in the State of Rondônia, Brazil. Semina: Ciencias Agrárias, v.37, n.5, p.3639-3646, 2016. Available from: <Available from: https://doi.org/10.5433/1679-0359.2016v37n5Supl2p3639 >. Accessed: Mar. 20, 2019. doi: 10.5433/1679-0359.2016v37n5Supl2p3639.
https://doi.org/10.5433/1679-0359.2016v3... ).

In the absence of epidemiological surveys, evaluations performed by disease control programs are often limited (TEBUG et al., 2014TEBUG, S. F. et al. Risk, knowledge and preventive measures of smallholder dairy farmers in northern Malawi with regard to zoonotic brucellosis and bovine tuberculosis. The Onderstepoort Journal of Veterinary Research, v.81, n.1, 2014. Available from: <Available from: https://doi.org/10.4102/ojvr.v81i1.594 >. Accessed: Mar. 20, 2019. doi: 10.4102/ojvr.v81i1.594.
https://doi.org/10.4102/ojvr.v81i1.594... ). Therefore, secondary data, which are provided by qualified Veterinarians, are essential in assessing health measures, allowing rapid generation of hypotheses and supporting decision-making. Using these data can result in optimizing resources and efficiency, such as in the monitoring and surveillance systems of animal health programs (TODESCHINI et al., 2018TODESCHINI, B. et al. Ocorrência de brucelose e tuberculose bovinas no Rio Grande do Sul com base em dados secundários. Pesquisa Veterinária Brasileira, v.38, n.1, p.15-22, 2018. Available from: <Available from: https://doi.org/10.1590/S0100-736X2018000100003 >. Accessed: Mar. 20, 2019. doi: 10.1590/S0100-736X2018000100003.
https://doi.org/10.1590/S0100-736X201800... ; RIBEIRO et al., 2020RIBEIRO, C. M. et al. Spatial and temporal trend analysis of bovine brucellosis in Brazil, 2014 to 2018. Semina: Ciências Agrárias, v.41, n.4, p.1279, 2020. Available from: <Available from: https://doi.org/10.5433/1679-0359.2020v41n4p1279 >. Accessed: Jun. 06, 2023. doi: 10.5433/1679-0359.2020v41n4p1279.
https://doi.org/10.5433/1679-0359.2020v4... ).

Considering the importance of PNCEBT in ensuring the beef and milk production chain and the lack of epidemiological surveys on bovine tuberculosis in the state, this study determined the frequency of animals an0d establishments positive for bovine tuberculosis in RN from June 2012 to December 2021.

MATERIALS AND METHODS

The state of RN has 167 municipalities, and, according to the Instituto de Defesa e Inspeção Agropecuária do Rio Grande do Norte (IDIARN), they are divided into 12 Unidade Local de Sanidade Animal e Vegetal (ULSAV), i.e., Assú, Caicó, Currais Novos, João Câmara, Mossoró, Nova Cruz, Umarizal, Santa Cruz, São Paulo do Potengi, Parnamirim, Pau dos Ferros, and Lajes (Figure 1).

Figure 1
Unidade Local de Sanidade Animal e Vegetal (ULSAV’S).

Secondary data provided by IDIARN were used, resulting from all monthly state reports issued by the 65 MVH for actions within the scope of PNCEBT by the Ministry of Agriculture, Livestock, and Supply (MAPA) of the different ULSAV. The data cover the period from June 2012 to December 2021.

For the diagnosis of Mycobacterium bovis infection, the comparative cervical test (CCT) was used as a routine and confirmatory test, according to the conditions and criteria established by PNCEBT (BRASIL, 2017BRASIL. Instrução Normativa SDA n°10, de 3 de Março de 2017. Ministério da Agricultura, Pecuária e Abastecimento. Secretaria de Defesa Animal, 2017. Accessed: Ago. 13, 2018.). A property was considered positive (focused) if at least one animal responded to the test.

Microsoft Excel 2013 was used to calculate the frequencies of positive animals and establishments per unit. Fisher’s exact test was performed with a significance level of 5 % (P < 0.05) to verify the association between the positive tuberculin skin test and sex (female and male). The tests were performed in the R environment (R CORE TEAM, 2020R CORE TEAM. R: A language and environment for statistical computing. R Foundation for Statistical Computing 2020. Available from: <Available from: https://www.R-project.org/ >. Accessed: Oct. 24, 2023.
https://www.R-project.org/... ) using the “rstatix” package (KASSAMBARA, 2021KASSAMBARA, A. 2021. rstatix: pipe-ffyramework for Basic Statistical Tests. R package version 0.7.0. Available from: <Available from: https://CRAN.R-project.org/package=rstatix >. Accessed: Oct. 24, 2023.
https://CRAN.R-project.org/package=rstat... ).

RESULTS AND DISCUSSION

Of the 45,804 cattle tested, 53 (0.1%) tested positive in the tuberculin skin test. Of the 44,722 females, 50 (0.1%) tested positive, while of the 1,082 males, three (0.2%) tested positive (Table 1). Using Fisher’s exact test, no differences were observed in the frequency of positivity between females and males at a significance level of 5% (P = 0.1298), with an odds ratio of 2.48 (95% CI, 0.5-7.71), and females representing 97.6% of all animals tested. In the establishment, 4,100 cattle were tested for bovine tuberculosis, with a frequency of 0.7% (Table 2).

Secondary data may enable the generation of consistent hypotheses about diseases, especially in the absence of broader studies, such as official epidemiological surveys, which; although, were more appropriate in most cases, requiring a lot of resources and presenting difficulties in their elaboration. However, they have some limitations, such as intrinsic biases, internal quality, and inferential limits (TODESCHINI et al., 2018TODESCHINI, B. et al. Ocorrência de brucelose e tuberculose bovinas no Rio Grande do Sul com base em dados secundários. Pesquisa Veterinária Brasileira, v.38, n.1, p.15-22, 2018. Available from: <Available from: https://doi.org/10.1590/S0100-736X2018000100003 >. Accessed: Mar. 20, 2019. doi: 10.1590/S0100-736X2018000100003.
https://doi.org/10.1590/S0100-736X201800... ). Furthermore, according to IDIARN, it is not possible to state that all animals were tested only once.

The study showed a low frequency of positive animals, 53 (0.1%) testing positive for tuberculosis. Similar results were observed in the state of Paraíba, where 54,472 cattle were tested and 136 (0.25%) were positive (FIGUEIREDO et al., 2010FIGUEIREDO, S. M. et al. Tuberculose bovina no Estado da Paraíba: Estudo retrospectivo. Pesquisa Veterinária Brasileira, v.2001, n.9, p.9-16, 2010. Available from: <Available from: https://doi.org/10.1590/S0100-736X2010000900002 >. Accessed: Mar. 20, 2019. doi: 10.1590/S0100-736X2010000900002.
https://doi.org/10.1590/S0100-736X201000... ). Superior results were observed in a survey in Rio Grande do Sul, where 62,149 cattle were tested with a positivity frequency of 0.87% was detected (TODESCHINI et al., 2018TODESCHINI, B. et al. Ocorrência de brucelose e tuberculose bovinas no Rio Grande do Sul com base em dados secundários. Pesquisa Veterinária Brasileira, v.38, n.1, p.15-22, 2018. Available from: <Available from: https://doi.org/10.1590/S0100-736X2018000100003 >. Accessed: Mar. 20, 2019. doi: 10.1590/S0100-736X2018000100003.
https://doi.org/10.1590/S0100-736X201800... ).

The highest frequencies of positive animals (Figure 2) were observed in the ULSAV of Santa Cruz, Currais Novos, and Caicó (0.3%, 0.3%, and 0.2%, respectively). These observed frequencies may be related to the presence of dairy herds in ULSAV. They produce approximately 46% of all bovine milk in RN (IBGE, 2017IBGE. Censo Agropecuário 2017. 2017. Available em: <Available em: https://censoagro2017.ibge.gov.br/templates/censoagro/resultadosagro/pecuaria >. Accessed: Aug. 13, 2018.
https://censoagro2017.ibge.gov.br/templa... ). In addition to the ULSAV in Santa Cruz and Caicó, the São Paulo do Potengi unit, which has properties with tuberculosis-free certification and increased tests, presented the highest frequencies of positive establishments. The results of this study were consistent with the study by NETO et al. (2016), who observed that the highest prevalence rates of infected herds and bovines that tested positive in the tuberculin skin test were found in the state of Espírito Santo, north of São Paulo, south of Minas Gerais, and south of Goiás, the Brazilian milk-producing zone.

Figure 2
Distribution of the frequency of animals that tested positive by units in the state of Rio Grande do Norte, from June 2012 to December 2021.

In this study, it was observed that during the study period, the ULSAV from Umarizal had the highest number of animals tested (6,722 animals), while the ULSAV from Nova Cruz tested only 1,008 bovines. This difference may be associated with some factors, such as the increased number of qualified veterinarians working in the municipalities that comprised the first ULSAV, in addition to the widespread dissemination of the program by the local team, raising awareness among breeders.

It should be noted that in the state of RN, cattle farming predominantly comprises dairy herds and 79% of the breeders are family farmers. These establishments account for 44% of the state’s production of bovine milk (SEPLAN, 2016bSECRETARIA DE ESTADO DO PLANEJAMENTO E DAS FINANCIAS (SEPLAN), 2016b. Edital N° 005/2016 - PROJETO RN SUSTENTÁVEL. Chamada Pública a Projetos de Apoio a Cadeia Produtiva do Leite e Derivados da Agricultura Familiar. Available from: <Available from: http://www.rnsustentavel.rn.gov.br >. Accessed: Feb. 09, 2023.
http://www.rnsustentavel.rn.gov.br... ). As a result, the state government has been financing projects related to milk production and its derivatives, in order to, introduce these products into the market and help agriculture industries (cheesemaking) adapt to family agriculture (SEPLAN, 2016aSECRETARIA DE ESTADO DO PLANEJAMENTO E DAS FINANCIAS (SEPLAN), 2016a. Diagnóstico e Planejamento Estratégico para o Desenvolvimento de Atividades Produtivas Agrícolas do Rio Grande do Norte. Available from: <Available from: http://www.rnsustentavel.rn.gov.br. >. Accessed: Aug. 13, 2018.
http://www.rnsustentavel.rn.gov.br.... ).

CONCLUSION

Measures that include raising awareness among producers, sanitary control in the acquisition and sale of cows for reproduction, inspection of sanitary barriers, and conducting epidemiological surveys to understand the actual situation of this disease in the state of RN are crucial.

ACKNOWLEDGMENTS

To the Instituto de Defesa e Inspeção Agropecuária do Rio Grande do Norte (IDIARN), for making secondary data available.

REFERENCES

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