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An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal
JIPH-251; No. of Pages 7
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Journal of Infection and Public Health (2013) xxx, xxx—xxx
An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal J. García Díez a,∗, A.C. Coelho b a
Cooperativa Agrícola de Chaves, ADS Vila Pouca de Aguiar, Bairro da Brangada, 5450-005 Vila Pouca de Aguiar, Portugal b Departamento das Ciências Veterinárias, CECAV, Universidade de Trás-os-Montes e Alto Douro, Apartado 1013, 5001-911 Vila Real, Portugal Received 11 February 2013 ; received in revised form 21 March 2013; accepted 19 April 2013
KEYWORDS Brucellosis; Cattle; Biosecurity; Education; Farmers
∗
Summary Little information is available regarding the connection between the risk of brucellosis infection in cattle and the lack of training and education of cattle producers. A total of 154 cattle farmers from the Vila Real (northern Portugal) municipality were interviewed in person to evaluate their knowledge of bovine brucellosis. Basic knowledge of the zoonotic characteristics and clinical signs of brucellosis infection and cattle management was obtained from 78.6%, 68.8% and 79.9% of the respondents, respectively. The respondents with infected animals in their herds (odds ratio (OR) 5.5; 95% confidence interval 1.6, 19.5) were more likely to have greater knowledge about bovine brucellosis. The study also revealed a relationship (p < 0.01) between the use of breeding males and farms that were already infected with brucellosis. Moreover, the knowledge that brucellosis is a zoonotic disease was also influenced by the number of farms already infected with brucellosis (p < 0.01). Conversely, the number of respondents who were unaware that bovine brucellosis is a zoonotic disease (25.3%) and a foodborne pathogen (21.4%), and the fact that over half (54.5%) of the respondents believed that bovine brucellosis was a treatable infectious disease was associated with the absence of veterinary assistance on the farm (60.4%). Because the eradication of bovine brucellosis has multiple factors, the success of the national eradication program cannot be based only on the sanitary management of infected herds. Successful eradication will only occur with adequate training programs for farmers, including farm biosecurity, legal fulfillment and veterinary public health programs (in which the role of the veterinarian is fundamental). © 2013 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Ltd. All rights reserved.
Corresponding author. Tel.: +351 259417782; fax: +351 259417376. E-mail address: [email protected] (J.G. Díez).
1876-0341/$ — see front matter © 2013 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jiph.2013.04.008
Please cite this article in press as: Díez JG, Coelho AC. An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal. J Infect Public Health (2013), http://dx.doi.org/10.1016/j.jiph.2013.04.008
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J.G. Díez, A.C. Coelho
Introduction
Materials and methods
Brucella spp. are facultative intracellular Gramnegative coccobacilli. These non-spore-forming and non-capsulated bacteria cause a serious contagious disease that results in reproductive failure and that has profound public health significance because of its zoonotic characteristics [1,2]. In cattle, Brucella abortus is the usual cause of brucellosis, but other Brucella spp., such as Brucella melitensis and Brucella suis, can (in rare cases) infect cattle [3]. The eradication of brucellosis in animals is a necessary step in controlling the disease in humans [4]. In cattle, during animal production, the infection causes heavy economic losses resulting from clinical disease, abortion, neonatal losses, increased calving intervals, reduced fertility, decreased milk production, increased culling rates because of metritis and the emergency slaughtering of infected animals [5,6]. In addition, the disease is an impediment to free animal movement and trade [7]. In Portugal, brucellosis control is mandatory [8]. All cattle older than 12 months are subjected to annual serological testing. Positive animals are culled when both the Rose Bengal and complement fixation tests are positive. Then, samples from several organs are taken at the slaughterhouse for bacteriological isolation. In infected flocks, special measures are performed at the farm, such as an epidemiological survey, cattle movement restriction and (at minimum) four serological tests within a 240-day period [9]. As an additional measure, serological testing (a premovement test) is compulsory for all bovine older than 12 months; before they leave the farm [10], calves younger than 12 months are slaughtered if they are the descendants of those cattle previously found to be positive. The potential risk factors for bovine brucellosis seroprevalence have been determined by epidemiological studies [11—13]. Several factors, such as gender, breed, age, herd size and management, ecological conditions and socioeconomic factors play an important but poorly defined role [14]. In Portugal, the risk factors of bovine brucellosis have not been previously investigated. Husbandry, grazing, hygiene, milking procedures, veterinary management and/or biosecurity measures are strongly associated with the training and education of farmers. Brucellosis control cannot rely only on test-and-slaughter programs, cattle producers should also be involved; therefore, as an important part of bovine brucellosis control, the aim of this study was to evaluate the farmers’ knowledge of bovine brucellosis.
Survey design A cross-sectional study of bovine brucellosis knowledge was conducted from April to July 2012. A voluntary survey (comprised of personal interviews) was administered to 154 cattle farmers of the Vila Real municipality, in northeast Portugal. The questionnaire was based on a literature review, and the questions were designed to obtain information about bovine brucellosis. Several questions were related to the respondents’ demographic characteristics (gender, age and education level) and information about their farms. The participants’ overall knowledge of bovine brucellosis was assessed using 18 closed questions. The responses to these questions were combined to generate a knowledge score ranging from zero to 18. After assessing the normality of the scores using a histogram, the composite score was dichotomized using the mean as a cut-off value; therefore, a value coded > one showed higher overall knowledge. A score of one was given to correct responses, and zero was used for incorrect and ‘‘I do not know’’ responses. Based on the mean score of the composite variable (mean = 9.85), the responses were categorized as high (a score above the mean value) and low (a score below the mean value). To reduce the possibility of farmers answering correctly by chance, all questions included the item ‘‘I do not know’’. During the interview, any herd could have been declared brucellosis positive by veterinary officials.
Pilot study A pilot study was conducted to assess the clarity of the questionnaire instructions, layout and time requirement. The pilot questionnaire was administered to 25 bovine farmers from the Sabrosa and Alijó municipalities in northeast Portugal. The results of this work are not included in this study.
Data analysis All questionnaire data were entered into an SPSS 19.0 database (SPSS, IBM, New York, USA) and carefully checked; the errors were corrected, and the data were immediately available as an SPSS dataset. All recorded information from each herd was carefully compared with the paper questionnaire and checked; typing errors were detected and corrected.
Please cite this article in press as: Díez JG, Coelho AC. An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal. J Infect Public Health (2013), http://dx.doi.org/10.1016/j.jiph.2013.04.008
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An evaluation of cattle farmers’ knowledge of bovine brucellosis The distributions of associated factors among those farmers who had more knowledge in bovine brucellosis and those with less knowledge were calculated. A multivariate logistic regression analysis was used to model the odds ratio (OR) and the confidence interval (CI, 95%) of having more knowledge related to the variables. The outcome variable was dichotomized into a high level of knowledge versus a low level, as a method of identifying any factors associated with knowledge. The potential associated factors (significant at p < 0.10, two-tailed, alpha = 0.05) in the univariate analysis were then evaluated using stepwise regression to construct a multivariate model (Wald test stepwise p-Wald value to enter p < 0.05). The multivariate logistic model was developed using the stepwise approach. A backward elimination followed by a forward selection for each variable was conducted using a likelihood ratio test at each step with 0.05 (two-tailed; alpha = 0.05) as a significant level for removal or entry. The fit of the model was assessed using the Hosmer and Lemeshow goodness-of-fit test [15]. The model was rerun until all remaining variables presented statistically significant values (p < 0.05).
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operated by both women and men working together (63.6%). Regarding respondent education, 71.4% had only primary educations, and 2.6% had high school educations or technical training.
Farm characterization The results of the farm characterization (Table 2) revealed that the main animal production was meat (94.2%). The majority of the respondents (57.8%) had three or fewer head, similar to the characteristics of most farms in this study. The average herd size was as follows: three head (18%), two head (22.1%) and one head (16.9%). Only 10% of respondents had over 10 head (range, 10—30 head). The other farm animals commingling with the cattle included sheep (11%), goats (9.1%), swine (4.5%), chickens (29.2%) and rabbits (15.6%). The examination of veterinary farm management revealed that 82.5% of the respondents had no knowledge of their official herd sanitary statuses; over half of the farms (60.4%) had no veterinary technical support, and 69.5% of the respondents requested veterinary technical support only when necessary.
General knowledge about bovine brucellosis
Results Farmer socio-demographic composition A total of 154 cattle farmers were interviewed (Table 1). The sample set consisted of 132 men (85.7%) and 22 women (14.3%). All respondents lived at the farm location and were older than 51 years (74%) on average. The farms were generally
According to the survey, 16.2% of respondents had experienced brucellosis infection in their herd (at least once), and 4.5% of the farmers had personally suffered brucellosis. Of the respondents, 77.3% believed that brucellosis was an infectious animal disease, and 74.7% believed it was a zoonotic disease; 83.8% answered that brucellosis was diagnosed with a serological test at a laboratory during
Table 2 Table 1 Socio-demographic characteristic of the respondent.
Gender Male Female Animal and farm operations Male Female Both Age <30 31—50 >51 Level of education Primary school High school or technical training
n
%
132 22
85.7 14.3
34 22 98
22.1 14.3 63.6
4 36 114
2.6 23.4 74.0
110 4
71.4 2.6
Farm characterization. n
Main animal production Meat 145 Milk 3 Both 6 Presence of others farm animals Sheep 11 Goat 14 Swine 7 Chicken 45 Rabbit 24 Herd sanitary status Known 27 Unknown 127 Veterinary assistance Yes 61 No 93
% 94.2 1.9 3.9 7.1 9.1 4.5 29.2 15.6 17.5 82.5 39.6 60.4
Please cite this article in press as: Díez JG, Coelho AC. An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal. J Infect Public Health (2013), http://dx.doi.org/10.1016/j.jiph.2013.04.008
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the official campaign or by a pre-movement test. Conversely, over half of the respondents (54.5%) believed that bovine brucellosis was a treatable infectious disease. Approximately three-quarters (78.6%) of the respondents recognized that non-heat treated milk was a source of infection. An investigation of the respondents’ knowledge of disease transmission revealed that grazing (63.6%) and pasture fecal contamination by infected animals were potential sources of transmission (64.3%). In addition, 79.9% of the respondents quarantined the infected animals. Questions regarding reproductive management showed that 60.4% of the respondents considered breeder males from non-free brucellosis herds or from herds of unknown status to be a potential source of brucellosis infection. In total, 66.2% of the farmers keep herds separate during the parturition period, and 68.2% hygienically removed the placentas. In addition, the presence of abortions was recognized as a sign of brucellosis (68.8%); when abortions occurred, 62.3% of respondents reported them to the official veterinary service. An association was found between the farms that had already undergone brucellosis and the correct response that breeder males were a high risk for brucellosis (p < 0.01) and also with the respondents who correctly answered that brucellosis is a zoonotic disease (p < 0.01). However, gender, age and education did not influence the presence of brucellosis on a farm and the general knowledge of the disease. Thus, veterinary technical support was not influenced by either the farmers’ education levels (p > 0.05) or the farms that had already undergone brucellosis.
Factors associated with the level of knowledge The possible factors associated with the farmers’ knowledge level of bovine brucellosis were evaluated. In the univariate analysis, three variables were found to be statistically significant when associated with the farmer’s knowledge of bovine brucellosis: the presence of goats on the farms, main animal production and previous herd infection. These variables were included in the multivariate model. To adjust for confounding factors, a backward stepwise conditional logistic regression was employed using the aforementioned statistically significant variables. After the stepwise procedure, only one variable was found to be significant (p < 0.05) in the multivariate logistic regression analysis of the OR for the knowledge of
bovine brucellosis in relation to the above reported associated factors. In this study, the farmers who had infected animals in their herds (OR 5.5; 95% CI 1.6, 19.5) had a higher probability of bovine brucellosis knowledge. The overall data of the model was: 2LL = 34,375; Hosmer and Lemeshow Chi-squared = 0.430; p = 0.51, degrees of freedom (df) = 1.
Discussion This study is the first to examine farmers’ knowledge of bovine brucellosis in northeast Portugal; it can be used as a tool to improve the bovine brucellosis national eradication program. The official data of bovine brucellosis in northeast Portugal increased from 2007 to 2009 with a household prevalence ranging from 0.32% to 0.71%, while the animal prevalence ranged from 0.15% to 0.31%. However, in 2010, the household and animal prevalences decreased to 0.59% and 0.227%, respectively. Although bovine brucellosis is considered controlled, new strategies must be developed to achieve its eradication. Thus, the knowledge/education of cattle producers may be fundamental in achieving this objective. In Portugal, brucellosis research is scarce and focused only on small ruminants [16,17]. According to our study results, approximately three-quarters of the respondents were older than 51 years and had low education/training; however, neither age nor education influenced the knowledge of the most important characteristics of bovine brucellosis. In contrast, younger age and higher education levels have been described as protective effects against brucellosis [18]. Although our results may be difficult to explain, they could be associated with the increased experience of the older farmers. This study showed that the farmers who had previously experienced brucellosis in their herds had a higher probability of having greater knowledge of bovine brucellosis, which was also consistent with having knowledge obtained from experience with the disease. Questions regarding the zoonotic characteristics and transmission sources of the disease were correctly answered by the majority of respondents. This knowledge reflected the decrease in human brucellosis cases in northeast Portugal over the last several years [19] because livestock production organizations have played an essential role in planning and executing a bovine brucellosis national eradication program and farmer education. Thus, 83.8% of the respondents recognized the objective
Please cite this article in press as: Díez JG, Coelho AC. An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal. J Infect Public Health (2013), http://dx.doi.org/10.1016/j.jiph.2013.04.008
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An evaluation of cattle farmers’ knowledge of bovine brucellosis and importance of the sanitary campaigns. Controlling brucellosis in a herd requires a biosecurity plan; consequently, farmer training is fundamental. Biosecurity refers to the measures taken to keep diseases out of populations, herds, or groups of animals in which they do not currently exist or to limit the spread of disease within the herd [20]. Among these measures, the control of animal movement, fulfillment of brucellosis policy and good husbandry practices are essential to brucellosis control. The cattle movement is controlled by the official veterinary service and restricted to brucellosispositive farms. A compulsory pre-movement test in all cattle older than one year increases the control of brucellosis; however, the benefits of this test are not entirely clear [21]. Although this measure is an economic constraint because of the pre-movement test cost, 70.8% of respondent agree with this measure [22]. In contrast, a deficient isolation and/or quarantine period of purchased cattle (to prevent dissemination of other diseases than brucellosis) was described in this part of the study [23]. The questions regarding reproductive management showed that approximately 70% of the farmers considered abortion to be a clinical sign of bovine brucellosis. In addition, 66.2% kept dams away during parturition, and 68.2% recognized the need for the proper disposal of placentas. This measure is important in intensive or semi-intensive animal production to avoid pasture contamination [24]; however, the farmers’ main objective was to increase comfort and prevent animal stress during this period. In addition, farmers must record all cases of abortions and report these incidents to the official veterinary service; over half of the respondents (62.3%) recognized the need for compliance with this measure. Conversely, 25.3% of respondents did not know that bovine brucellosis is a zoonotic disease; 21.4% did not know that consumption of raw milk may be a source of infection, and over half (54.5%) considered bovine brucellosis to be a treatable infectious disease, although it is strictly prohibited by law. These results were associated with the absence of a veterinarian on the farm (60.4%), but approximately three-quarters (69.5%) of the respondents requested a veterinarian only in the case of sick cattle. The role of a veterinarian in the education/training of cattle producers is essential for improving the understanding not only of the sanitary aspects but also of issues about farm biosecurity, veterinary legal fulfillment and veterinary public health [25]. To achieve better results, collaboration with human public health personnel may be important.
Table 3 General brucellosis.
5 knowledge n
about
bovine %
Herd infected Yes 25 16.2 No 108 70.1 Not known 21 13.6 Farmer infected by brucellosis Yes 7 4.5 No 128 83.1 Not known 19 12.3 Brucellosis as an infectious disease Yes 119 77.3 No 7 4.5 Not known 28 18.2 Bovine brucellosis as a zoonotic disease Yes 115 74.7 No 12 7.8 Not known 27 17.5 Bovine brucellosis diagnosis by serological test Yes 129 83.8 No 6 3.9 Not known 19 12.3 Brucellosis as a treatable disease Yes 84 54.5 No 40 26.0 Not known 30 19.5 Raw milk consumption as source of brucellosis Yes 121 78.6 No 9 5.8 Not known 24 15.6 Cattle infection in the pasture Yes 98 63.6 No 25 16.2 Not known 31 20.1 Isolation of infected cattle Yes 123 79.9 No 11 7.1 Not known 20 13.0 Lend male increase risk of bovine brucellosis Yes 93 60.4 No 23 14.9 Not known 38 24.7 Isolation of dams during calving Yes 102 66.2 No 24 15.6 Not known 28 18.2 Proper disposal of placentas Yes 68.2 68.2 No 9 5.8 Not known 40 26.0 Abortion as a clinical sign of bovine brucellosis Yes 106 68.8 No 13 8.4 Not known 35 22.7 Communication of abortion to official veterinary services Yes 96 62.3 No 29 18.8 Not known 29 18.8
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Conclusion Farmers’ knowledge of bovine brucellosis is an important tool for improving the official eradication program. According to our study results, farmers have a good knowledge of bovine brucellosis despite age and/or lack of training. This knowledge can be explained by the fact that brucellosis is officially controlled and because of previous efforts by the livestock producers organization. In contrast, farm biosecurity knowledge was deficient because it is not mandatory, and no veterinary technical support was required by farmers. Conversely, the lack of understanding that bovine brucellosis is a zoonotic disease and/or a foodborne pathogen, in addition to its consideration as a treatable infectious disease, could be associated with the absence of veterinary assistance on farms (Table 3). To avoid this problem, brucellosis control and eradication must be associated with farmers’ training programs. These training programs should teach sanitary management, farm biosecurity, legal fulfillment and veterinary public health, in which the role of the veterinarian is fundamental.
Conflict of interest Funding: No funding sources. Competing interests: None declared. Ethical approval: Not required.
Acknowledgements The authors would like to thank all survey respondents. This work was supported by the strategic research project PEst-OE/AGR/UI0772/2011 financed by the Foundation for Science and Technology (FCT).
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[5] Carvalho Neta AV, Mol JPS, Xavier MN, Paixão TA, Lage AP, Santos RL. Pathogenesis of bovine brucellosis. The Veterinary Journal 2010;184:146—55. [6] Radostits OM, Gay CC, Blood D, Hinchcliff KW. Medicina Veterinaria — Tratado de enfermedades del ganado bovino, ovino, porcino, caprino y equino. 9th ed. Madrid: McGrawHill Interamericana; 2000. [7] Portugal. Decreto-Lei n◦ . 142/2006 de 27 de Julho; 2006. [8] Portugal. Decreto-Lei n.◦ 244/2000 de 27 de Setembro; 2000. [9] DGV — Direcc ¸ão Geral de Veterinária. Programa de erradicac ¸ão da brucelose dos bovinos em Portugal — 2012. Lisboa: Ministério de Agricultura, Mar, Ambiente e Ordenamento do Território; 2011. [10] DGAV — Direcc ¸ão Geral de Alimentac ¸ão e Veterinária. Manual de Apoio à implementac ¸ão dos testes prémovimentac ¸ão em território nacional no âmbito dos ¸ão da tuberculose e brucelose bovprogramas de erradicac ina; 2012. [11] Dalla Pozza M, Martín M, Marangon S, Manca G, Ricci A. A case—control study of risk factors for bovine brucellosis in the Veneto region (Italy). Epidemiologie et Santé Animale 1997;31-32:11041—3. [12] Sanogo M, Abatih E, Thys E, Fretin D, Berkvens D, Saegerman C. Risk factors associated with brucellosis seropositivity among cattle in the central savannahforest area of Ivory Coast. Preventive Veterinary Medicine 2012;107:51—6. [13] Stringer LA, Guitian FJ, Abernethy DA, Honhold NH, Menzies FD. Risk associated with animals moved from herds infected with brucellosis in Northern Ireland. Preventive Veterinary Medicine 2008;84:72—84. [14] Crespo F. Brucelosis ovina y caprina. Paris: O.I.E.; 1994. [15] Hosmer DW, Lemeshow S. Applied logistic regression. 2nd ed. New York: Wiley; 2000. [16] Coelho AM, Coelho AC, Roboredo M, Rodrigues J. A case—control study of risk factors for brucellosis seropositivity in Portuguese small ruminants herds. Veterinary Preventive Medicine 2007;82:291—301. [17] Lobo-Fenandes MO. Brucelose dos pequenos ruminantes: estudo de focos na área administrativa da Divisão de Intervenc ¸ão Veterinária de Vila Real 2012. Lisboa: Universidade Técnica de Lisboa — Faculdade de Medicina Veterinária; 2012. [18] Mainar-Jaime RC, Vázquez-Boland JA. Associations of veterinary services and farmer characteristics with the prevalences of brucellosis and border disease in small ruminants in Spain. Preventive Veterinary Medicine 1999;40: 193—205. [19] Doenc ¸as de declarac ¸ão obrigatória. 2004-2008. Direcc ¸ão de Servic ¸os de Epidemiologia e Estatísticas da Saúde — Divisão ¸ão-Geral da Saúde; 2010. de Epidemiologia. Lisboa: Direcc [20] Dargatz DA, Garry FB, Traub-Dargatz JL. An introduction to biosecurity of cattle operations. The Veterinary Clinics Food Animal Practice 2002;18:1—5. [21] Clegg TA, More SJ, Higgins IM, Good M, Blake M, Williams DH. Potential infection-control benefit for Ireland from premovement testing of cattle for tuberculosis. Preventive Veterinary Medicine 2008;84:94—111. [22] Christley RM, Robinson SE, Moore B, Setzkorn C, Donald I. Responses of farmers to introduction in England and Wales of pre-movement testing for bovine tuberculosis. Preventive Veterinary Medicine 2011;100:126—33. [23] García-Díez J. Evaluación de la seguridad alimentaria en na y mediexplotaciones de vacuno lechero de peque˜ ana dimensión en los municipios de Vila Real y Sabrosa (Portugal) a través de la aplicación de prácticas correctas y
Please cite this article in press as: Díez JG, Coelho AC. An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal. J Infect Public Health (2013), http://dx.doi.org/10.1016/j.jiph.2013.04.008
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An evaluation of cattle farmers’ knowledge of bovine brucellosis medidas de bioseguridad. Revista Electrónica de Veterinaria 2012;13:1—14. [24] Havas KA, Ramishvil M, Navdarashvili A, Imnadze P, Salman M. The human—animal interface of domestic livestock management and production and its relationship to brucellosis
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in the country of Georgia: a rapid assessment analysis. Preventive Veterinary Medicine 2012;105:10—6. [25] Cripps PJ. Veterinary education, zoonoses and public health: a personal perspective. Acta Tropica 2000;76:77—80.
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Journal of Infection and Public Health (2013) xxx, xxx—xxx
An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal J. García Díez a,∗, A.C. Coelho b a
Cooperativa Agrícola de Chaves, ADS Vila Pouca de Aguiar, Bairro da Brangada, 5450-005 Vila Pouca de Aguiar, Portugal b Departamento das Ciências Veterinárias, CECAV, Universidade de Trás-os-Montes e Alto Douro, Apartado 1013, 5001-911 Vila Real, Portugal Received 11 February 2013 ; received in revised form 21 March 2013; accepted 19 April 2013
KEYWORDS Brucellosis; Cattle; Biosecurity; Education; Farmers
∗
Summary Little information is available regarding the connection between the risk of brucellosis infection in cattle and the lack of training and education of cattle producers. A total of 154 cattle farmers from the Vila Real (northern Portugal) municipality were interviewed in person to evaluate their knowledge of bovine brucellosis. Basic knowledge of the zoonotic characteristics and clinical signs of brucellosis infection and cattle management was obtained from 78.6%, 68.8% and 79.9% of the respondents, respectively. The respondents with infected animals in their herds (odds ratio (OR) 5.5; 95% confidence interval 1.6, 19.5) were more likely to have greater knowledge about bovine brucellosis. The study also revealed a relationship (p < 0.01) between the use of breeding males and farms that were already infected with brucellosis. Moreover, the knowledge that brucellosis is a zoonotic disease was also influenced by the number of farms already infected with brucellosis (p < 0.01). Conversely, the number of respondents who were unaware that bovine brucellosis is a zoonotic disease (25.3%) and a foodborne pathogen (21.4%), and the fact that over half (54.5%) of the respondents believed that bovine brucellosis was a treatable infectious disease was associated with the absence of veterinary assistance on the farm (60.4%). Because the eradication of bovine brucellosis has multiple factors, the success of the national eradication program cannot be based only on the sanitary management of infected herds. Successful eradication will only occur with adequate training programs for farmers, including farm biosecurity, legal fulfillment and veterinary public health programs (in which the role of the veterinarian is fundamental). © 2013 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Ltd. All rights reserved.
Corresponding author. Tel.: +351 259417782; fax: +351 259417376. E-mail address: [email protected] (J.G. Díez).
1876-0341/$ — see front matter © 2013 King Saud Bin Abdulaziz University for Health Sciences. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jiph.2013.04.008
Please cite this article in press as: Díez JG, Coelho AC. An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal. J Infect Public Health (2013), http://dx.doi.org/10.1016/j.jiph.2013.04.008
JIPH-251; No. of Pages 7
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J.G. Díez, A.C. Coelho
Introduction
Materials and methods
Brucella spp. are facultative intracellular Gramnegative coccobacilli. These non-spore-forming and non-capsulated bacteria cause a serious contagious disease that results in reproductive failure and that has profound public health significance because of its zoonotic characteristics [1,2]. In cattle, Brucella abortus is the usual cause of brucellosis, but other Brucella spp., such as Brucella melitensis and Brucella suis, can (in rare cases) infect cattle [3]. The eradication of brucellosis in animals is a necessary step in controlling the disease in humans [4]. In cattle, during animal production, the infection causes heavy economic losses resulting from clinical disease, abortion, neonatal losses, increased calving intervals, reduced fertility, decreased milk production, increased culling rates because of metritis and the emergency slaughtering of infected animals [5,6]. In addition, the disease is an impediment to free animal movement and trade [7]. In Portugal, brucellosis control is mandatory [8]. All cattle older than 12 months are subjected to annual serological testing. Positive animals are culled when both the Rose Bengal and complement fixation tests are positive. Then, samples from several organs are taken at the slaughterhouse for bacteriological isolation. In infected flocks, special measures are performed at the farm, such as an epidemiological survey, cattle movement restriction and (at minimum) four serological tests within a 240-day period [9]. As an additional measure, serological testing (a premovement test) is compulsory for all bovine older than 12 months; before they leave the farm [10], calves younger than 12 months are slaughtered if they are the descendants of those cattle previously found to be positive. The potential risk factors for bovine brucellosis seroprevalence have been determined by epidemiological studies [11—13]. Several factors, such as gender, breed, age, herd size and management, ecological conditions and socioeconomic factors play an important but poorly defined role [14]. In Portugal, the risk factors of bovine brucellosis have not been previously investigated. Husbandry, grazing, hygiene, milking procedures, veterinary management and/or biosecurity measures are strongly associated with the training and education of farmers. Brucellosis control cannot rely only on test-and-slaughter programs, cattle producers should also be involved; therefore, as an important part of bovine brucellosis control, the aim of this study was to evaluate the farmers’ knowledge of bovine brucellosis.
Survey design A cross-sectional study of bovine brucellosis knowledge was conducted from April to July 2012. A voluntary survey (comprised of personal interviews) was administered to 154 cattle farmers of the Vila Real municipality, in northeast Portugal. The questionnaire was based on a literature review, and the questions were designed to obtain information about bovine brucellosis. Several questions were related to the respondents’ demographic characteristics (gender, age and education level) and information about their farms. The participants’ overall knowledge of bovine brucellosis was assessed using 18 closed questions. The responses to these questions were combined to generate a knowledge score ranging from zero to 18. After assessing the normality of the scores using a histogram, the composite score was dichotomized using the mean as a cut-off value; therefore, a value coded > one showed higher overall knowledge. A score of one was given to correct responses, and zero was used for incorrect and ‘‘I do not know’’ responses. Based on the mean score of the composite variable (mean = 9.85), the responses were categorized as high (a score above the mean value) and low (a score below the mean value). To reduce the possibility of farmers answering correctly by chance, all questions included the item ‘‘I do not know’’. During the interview, any herd could have been declared brucellosis positive by veterinary officials.
Pilot study A pilot study was conducted to assess the clarity of the questionnaire instructions, layout and time requirement. The pilot questionnaire was administered to 25 bovine farmers from the Sabrosa and Alijó municipalities in northeast Portugal. The results of this work are not included in this study.
Data analysis All questionnaire data were entered into an SPSS 19.0 database (SPSS, IBM, New York, USA) and carefully checked; the errors were corrected, and the data were immediately available as an SPSS dataset. All recorded information from each herd was carefully compared with the paper questionnaire and checked; typing errors were detected and corrected.
Please cite this article in press as: Díez JG, Coelho AC. An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal. J Infect Public Health (2013), http://dx.doi.org/10.1016/j.jiph.2013.04.008
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An evaluation of cattle farmers’ knowledge of bovine brucellosis The distributions of associated factors among those farmers who had more knowledge in bovine brucellosis and those with less knowledge were calculated. A multivariate logistic regression analysis was used to model the odds ratio (OR) and the confidence interval (CI, 95%) of having more knowledge related to the variables. The outcome variable was dichotomized into a high level of knowledge versus a low level, as a method of identifying any factors associated with knowledge. The potential associated factors (significant at p < 0.10, two-tailed, alpha = 0.05) in the univariate analysis were then evaluated using stepwise regression to construct a multivariate model (Wald test stepwise p-Wald value to enter p < 0.05). The multivariate logistic model was developed using the stepwise approach. A backward elimination followed by a forward selection for each variable was conducted using a likelihood ratio test at each step with 0.05 (two-tailed; alpha = 0.05) as a significant level for removal or entry. The fit of the model was assessed using the Hosmer and Lemeshow goodness-of-fit test [15]. The model was rerun until all remaining variables presented statistically significant values (p < 0.05).
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operated by both women and men working together (63.6%). Regarding respondent education, 71.4% had only primary educations, and 2.6% had high school educations or technical training.
Farm characterization The results of the farm characterization (Table 2) revealed that the main animal production was meat (94.2%). The majority of the respondents (57.8%) had three or fewer head, similar to the characteristics of most farms in this study. The average herd size was as follows: three head (18%), two head (22.1%) and one head (16.9%). Only 10% of respondents had over 10 head (range, 10—30 head). The other farm animals commingling with the cattle included sheep (11%), goats (9.1%), swine (4.5%), chickens (29.2%) and rabbits (15.6%). The examination of veterinary farm management revealed that 82.5% of the respondents had no knowledge of their official herd sanitary statuses; over half of the farms (60.4%) had no veterinary technical support, and 69.5% of the respondents requested veterinary technical support only when necessary.
General knowledge about bovine brucellosis
Results Farmer socio-demographic composition A total of 154 cattle farmers were interviewed (Table 1). The sample set consisted of 132 men (85.7%) and 22 women (14.3%). All respondents lived at the farm location and were older than 51 years (74%) on average. The farms were generally
According to the survey, 16.2% of respondents had experienced brucellosis infection in their herd (at least once), and 4.5% of the farmers had personally suffered brucellosis. Of the respondents, 77.3% believed that brucellosis was an infectious animal disease, and 74.7% believed it was a zoonotic disease; 83.8% answered that brucellosis was diagnosed with a serological test at a laboratory during
Table 2 Table 1 Socio-demographic characteristic of the respondent.
Gender Male Female Animal and farm operations Male Female Both Age <30 31—50 >51 Level of education Primary school High school or technical training
n
%
132 22
85.7 14.3
34 22 98
22.1 14.3 63.6
4 36 114
2.6 23.4 74.0
110 4
71.4 2.6
Farm characterization. n
Main animal production Meat 145 Milk 3 Both 6 Presence of others farm animals Sheep 11 Goat 14 Swine 7 Chicken 45 Rabbit 24 Herd sanitary status Known 27 Unknown 127 Veterinary assistance Yes 61 No 93
% 94.2 1.9 3.9 7.1 9.1 4.5 29.2 15.6 17.5 82.5 39.6 60.4
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the official campaign or by a pre-movement test. Conversely, over half of the respondents (54.5%) believed that bovine brucellosis was a treatable infectious disease. Approximately three-quarters (78.6%) of the respondents recognized that non-heat treated milk was a source of infection. An investigation of the respondents’ knowledge of disease transmission revealed that grazing (63.6%) and pasture fecal contamination by infected animals were potential sources of transmission (64.3%). In addition, 79.9% of the respondents quarantined the infected animals. Questions regarding reproductive management showed that 60.4% of the respondents considered breeder males from non-free brucellosis herds or from herds of unknown status to be a potential source of brucellosis infection. In total, 66.2% of the farmers keep herds separate during the parturition period, and 68.2% hygienically removed the placentas. In addition, the presence of abortions was recognized as a sign of brucellosis (68.8%); when abortions occurred, 62.3% of respondents reported them to the official veterinary service. An association was found between the farms that had already undergone brucellosis and the correct response that breeder males were a high risk for brucellosis (p < 0.01) and also with the respondents who correctly answered that brucellosis is a zoonotic disease (p < 0.01). However, gender, age and education did not influence the presence of brucellosis on a farm and the general knowledge of the disease. Thus, veterinary technical support was not influenced by either the farmers’ education levels (p > 0.05) or the farms that had already undergone brucellosis.
Factors associated with the level of knowledge The possible factors associated with the farmers’ knowledge level of bovine brucellosis were evaluated. In the univariate analysis, three variables were found to be statistically significant when associated with the farmer’s knowledge of bovine brucellosis: the presence of goats on the farms, main animal production and previous herd infection. These variables were included in the multivariate model. To adjust for confounding factors, a backward stepwise conditional logistic regression was employed using the aforementioned statistically significant variables. After the stepwise procedure, only one variable was found to be significant (p < 0.05) in the multivariate logistic regression analysis of the OR for the knowledge of
bovine brucellosis in relation to the above reported associated factors. In this study, the farmers who had infected animals in their herds (OR 5.5; 95% CI 1.6, 19.5) had a higher probability of bovine brucellosis knowledge. The overall data of the model was: 2LL = 34,375; Hosmer and Lemeshow Chi-squared = 0.430; p = 0.51, degrees of freedom (df) = 1.
Discussion This study is the first to examine farmers’ knowledge of bovine brucellosis in northeast Portugal; it can be used as a tool to improve the bovine brucellosis national eradication program. The official data of bovine brucellosis in northeast Portugal increased from 2007 to 2009 with a household prevalence ranging from 0.32% to 0.71%, while the animal prevalence ranged from 0.15% to 0.31%. However, in 2010, the household and animal prevalences decreased to 0.59% and 0.227%, respectively. Although bovine brucellosis is considered controlled, new strategies must be developed to achieve its eradication. Thus, the knowledge/education of cattle producers may be fundamental in achieving this objective. In Portugal, brucellosis research is scarce and focused only on small ruminants [16,17]. According to our study results, approximately three-quarters of the respondents were older than 51 years and had low education/training; however, neither age nor education influenced the knowledge of the most important characteristics of bovine brucellosis. In contrast, younger age and higher education levels have been described as protective effects against brucellosis [18]. Although our results may be difficult to explain, they could be associated with the increased experience of the older farmers. This study showed that the farmers who had previously experienced brucellosis in their herds had a higher probability of having greater knowledge of bovine brucellosis, which was also consistent with having knowledge obtained from experience with the disease. Questions regarding the zoonotic characteristics and transmission sources of the disease were correctly answered by the majority of respondents. This knowledge reflected the decrease in human brucellosis cases in northeast Portugal over the last several years [19] because livestock production organizations have played an essential role in planning and executing a bovine brucellosis national eradication program and farmer education. Thus, 83.8% of the respondents recognized the objective
Please cite this article in press as: Díez JG, Coelho AC. An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal. J Infect Public Health (2013), http://dx.doi.org/10.1016/j.jiph.2013.04.008
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An evaluation of cattle farmers’ knowledge of bovine brucellosis and importance of the sanitary campaigns. Controlling brucellosis in a herd requires a biosecurity plan; consequently, farmer training is fundamental. Biosecurity refers to the measures taken to keep diseases out of populations, herds, or groups of animals in which they do not currently exist or to limit the spread of disease within the herd [20]. Among these measures, the control of animal movement, fulfillment of brucellosis policy and good husbandry practices are essential to brucellosis control. The cattle movement is controlled by the official veterinary service and restricted to brucellosispositive farms. A compulsory pre-movement test in all cattle older than one year increases the control of brucellosis; however, the benefits of this test are not entirely clear [21]. Although this measure is an economic constraint because of the pre-movement test cost, 70.8% of respondent agree with this measure [22]. In contrast, a deficient isolation and/or quarantine period of purchased cattle (to prevent dissemination of other diseases than brucellosis) was described in this part of the study [23]. The questions regarding reproductive management showed that approximately 70% of the farmers considered abortion to be a clinical sign of bovine brucellosis. In addition, 66.2% kept dams away during parturition, and 68.2% recognized the need for the proper disposal of placentas. This measure is important in intensive or semi-intensive animal production to avoid pasture contamination [24]; however, the farmers’ main objective was to increase comfort and prevent animal stress during this period. In addition, farmers must record all cases of abortions and report these incidents to the official veterinary service; over half of the respondents (62.3%) recognized the need for compliance with this measure. Conversely, 25.3% of respondents did not know that bovine brucellosis is a zoonotic disease; 21.4% did not know that consumption of raw milk may be a source of infection, and over half (54.5%) considered bovine brucellosis to be a treatable infectious disease, although it is strictly prohibited by law. These results were associated with the absence of a veterinarian on the farm (60.4%), but approximately three-quarters (69.5%) of the respondents requested a veterinarian only in the case of sick cattle. The role of a veterinarian in the education/training of cattle producers is essential for improving the understanding not only of the sanitary aspects but also of issues about farm biosecurity, veterinary legal fulfillment and veterinary public health [25]. To achieve better results, collaboration with human public health personnel may be important.
Table 3 General brucellosis.
5 knowledge n
about
bovine %
Herd infected Yes 25 16.2 No 108 70.1 Not known 21 13.6 Farmer infected by brucellosis Yes 7 4.5 No 128 83.1 Not known 19 12.3 Brucellosis as an infectious disease Yes 119 77.3 No 7 4.5 Not known 28 18.2 Bovine brucellosis as a zoonotic disease Yes 115 74.7 No 12 7.8 Not known 27 17.5 Bovine brucellosis diagnosis by serological test Yes 129 83.8 No 6 3.9 Not known 19 12.3 Brucellosis as a treatable disease Yes 84 54.5 No 40 26.0 Not known 30 19.5 Raw milk consumption as source of brucellosis Yes 121 78.6 No 9 5.8 Not known 24 15.6 Cattle infection in the pasture Yes 98 63.6 No 25 16.2 Not known 31 20.1 Isolation of infected cattle Yes 123 79.9 No 11 7.1 Not known 20 13.0 Lend male increase risk of bovine brucellosis Yes 93 60.4 No 23 14.9 Not known 38 24.7 Isolation of dams during calving Yes 102 66.2 No 24 15.6 Not known 28 18.2 Proper disposal of placentas Yes 68.2 68.2 No 9 5.8 Not known 40 26.0 Abortion as a clinical sign of bovine brucellosis Yes 106 68.8 No 13 8.4 Not known 35 22.7 Communication of abortion to official veterinary services Yes 96 62.3 No 29 18.8 Not known 29 18.8
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Conclusion Farmers’ knowledge of bovine brucellosis is an important tool for improving the official eradication program. According to our study results, farmers have a good knowledge of bovine brucellosis despite age and/or lack of training. This knowledge can be explained by the fact that brucellosis is officially controlled and because of previous efforts by the livestock producers organization. In contrast, farm biosecurity knowledge was deficient because it is not mandatory, and no veterinary technical support was required by farmers. Conversely, the lack of understanding that bovine brucellosis is a zoonotic disease and/or a foodborne pathogen, in addition to its consideration as a treatable infectious disease, could be associated with the absence of veterinary assistance on farms (Table 3). To avoid this problem, brucellosis control and eradication must be associated with farmers’ training programs. These training programs should teach sanitary management, farm biosecurity, legal fulfillment and veterinary public health, in which the role of the veterinarian is fundamental.
Conflict of interest Funding: No funding sources. Competing interests: None declared. Ethical approval: Not required.
Acknowledgements The authors would like to thank all survey respondents. This work was supported by the strategic research project PEst-OE/AGR/UI0772/2011 financed by the Foundation for Science and Technology (FCT).
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