article: Rabies remains a disease of significant zoonotic and economic concern in rabies endemic areas of Bhutan. Rabies outbreaks in livestock threaten the livelihoods of subsistence farming communities and pose a potential public health threat. As a part of identifying approaches to prevent rabies in cattle, a Knowledge, Attitude, and Practice (KAP) survey was conducted among cattle owners in selected rural areas of the southern rabies high-risk zone and low-risk zone in eastern Bhutan. Between March and April 2017,562 cattle owners (281 in the east and 281 in the south) were interviewed using a questionnaire. Eighty-eight percent of the participants had heard of rabies but only 39% of the participants who had heard of rabies had adequate knowledge about rabies. Multivariable logistic regression analysis showed that residing in the south [OR = 9. 25 (95% CI: 6. 01–14. 53) ] and having seen a rabies case [OR = 2. 46 (95% CI: 1. 6–3. 82) ] were significantly associated with having adequate knowledge about rabies. Based on our scoring criteria, 65% of the total participants who had heard of rabies had a favorable attitude towards rabies control and prevention programs. The participants residing in the east were two times more likely to have a favourable attitude than their counterparts in the south [OR = 2. 08 (95% CI: 1. 43–3. 05) ]. More than 70% of the participants reported engaging in farm activities such as examining the oral cavity of sick cattle and assisting cattle during parturition. Only 25% of the participants reported using personal protective equipment while undertaking these activities. Despite a high level of rabies awareness, we observed that there is a lack of comprehensive knowledge about rabies regarding susceptible hosts, transmission routes, the health outcome of rabies infection in humans, and appropriate health-seeking behaviours. This study highlights the need to strengthen rabies education programs in rural communities to address the knowledge gaps that have been identified.
  Bhutan is a small Himalayan Kingdom located in South Asia bordered by India in the south, West, and East and the Autonomous region of Tibet in the North. Around 62. 2% of its population lives in rural areas and depends on subsistence agriculture and livestock farming [1]. Cattle (Bos indicus and Bos taurus) are the most commonly reared livestock in Bhutan [2], and they play an important role in sustaining rural livelihoods by serving as a source of food, manure, draught power, and as an immediate source of income. However, infectious diseases remain a threat to livestock production resulting in economic losses due to decreased productivity as well as death of affected animals. Common infectious diseases affecting cattle in Bhutan include foot and mouth disease, rabies, hemorrhagic septicaemia, black quarter, and anthrax. Rabies is one of the most important zoonotic diseases in Bhutan. Despite implementing control measures, the country continues to experience around 17 outbreaks in animals annually, especially in cattle [3]. The Department of Livestock (DoL) under the Ministry of Agriculture and Forests (MoAF) spearheads rabies control program in animals in Bhutan. Apart from conducting mass dog vaccination and animal birth control campaign, rabies awareness education is regularly disseminated to the public via television and radio programs and by observing World Rabies Day annually. Rabies outbreaks are mainly reported in the southern parts of Bhutan that share a porous border with the neighboring States of India -West Bengal and Assam. This is due to the cross-border movement of dogs [4]. Although the interior part of Bhutan is considered free from dog-mediated rabies, re-emergence of rabies has been observed in the recent past due to incursions of rabid dogs from the bordering towns. For instance, rabies had re-emerged during 2005 and 2016 in the eastern part of the country that share border with an Indian State of Arunachal Pradesh [5,6]. In Bhutan, rabies is most commonly reported in cattle as a result of spill over infection from dogs [7]. Consequently, several incidents of potential mass human exposure have been reported following handling of rabid animals and carcases during zoo-sanitary measures, and consumption of animal products derived from cattle suspected or confirmed of being infected with rabies [8]. Rabies in cattle results in direct economic losses to the farmers through the loss of cattle and their production, and there is also a cost to the government for responding to outbreaks and providing mass rabies PEP [9]. Although there is a comprehensive Government supported program in Bhutan to control rabies in dogs, no rabies prevention measures are implemented in cattle and other livestock in the rabies endemic areas of Bhutan. To plan appropriate intervention measures to prevent rabies outbreaks in cattle, and to avert subsequent economic losses and public health risks, it is imperative to understand cattle owners’ knowledge and perception about rabies, the prevalent on-farm practices that could predispose exposure to rabies in cattle. Previous community-based studies conducted amongst selected urban residents and dog owners in Bhutan have indicated a high level of awareness and knowledge about rabies [6,10]; however, no studies have been carried out targeting cattle owners and rural households. Therefore, the objectives of this study were to assess and compare the KAP regarding rabies among the cattle owners in selected rural areas of the southern high-risk rabies zone and a rabies low risk zone in the eastern Bhutan. Based on this study findings, a community-based education program will be implemented in the study areas and other identified communities to enhance prevention and control of rabies in humans and animals.
  Administratively, Bhutan is divided into 20 districts (dzongkhags) and 205 sub-districts (gewogs) (Fig 1). Several villages form a sub-district. In this study, two districts—Chukha and Trashigang—were selected based on convenience and purpose [11]. Chukha is a rabies endemic district, while Trashigang is not. Furthermore, as the Regional Livestock Development Centre (RLDC) were in Chukha and Trashigang, it was logistically convenient to recruit and train survey enumerators for the conduct of the study. The sub-districts of Phuentsholing and Sampheling were selected from Chukha district as these sub-districts reports the highest number of rabies outbreaks in animals every year. The sub-district of Kanglung under Trashigang district was included in the study as it falls under a rabies low-risk zone in eastern Bhutan [3]. At the time of our field survey no rabies outbreaks were reported in the southern study areas. However, in October 2016, few months before our study, a major rabies outbreak had occurred in five sub-districts under Trashigang [6]. One of these sub-districts was adjacent to Samkhar, one of our study areas in the east. The sample size required for comparing two populations was calculated using a web-based sample size calculator designed by the University of British Columbia, Canada (https: //www. stat. ubc. ca/~rollin/stats/ssize/b2. html). Since no studies were conducted previously in these selected areas, based on local knowledge, we assumed that 30% and 40% of the cattle owners would have knowledge and awareness about rabies in the eastern and southern areas, respectively. With a confidence level of 95% and the statistical power of 80%, 562 cattle owners (281 from each study area) were required to be selected and interviewed. Twenty-five villages from Phuentsholing and Samphelling, and all the 12 villages from Kanglung sub-district were selected for this study. The official lists of cattle owners in the selected study areas were collected from the respective District Livestock Offices and were used as the sampling frame. The required number of participants was drawn randomly using Microsoft Excel 2013 (Microsoft excel 2013, Redmond, USA) after assigning a random number to each cattle owner. However, during the field survey, it was observed that some of the selected participants did not own cattle anymore. Some had sold their cattle while others had not replaced their dead cattle. In such cases, the nearest cattle-owning household was selected. For the same reason, in the eastern region, 28 households were interviewed from a neighboring sub-district, Samkhar. In this paper, the southern rabies high-risk study site will be referred to as ‘south’ and the eastern rabies low-risk site as ‘east’. A questionnaire comprising five different sections was prepared and used for data collection. Section one comprised questions regarding the participants’ socio-demographic information. Sections two, three, and four comprised questions related to participants’ Knowledge, Attitude, and Practices regarding rabies, respectively. The questions used for collecting information in these four sections were all closed ended. The final section (section five) included both open and close ended questions to determine participants’ farm and farm production characteristics. Nine livestock personnel working in the Southern and Eastern RLDCs were recruited and trained as survey enumerators. The questionnaire was pretested during mock interviews that were carried out as a part of a survey enumerators’ training program and modified accordingly to improve clarity. The selected households who owned at least one cattle and one of the adult members in households who were 18 years and above, were included for the interview in this study. Prior to start of the interviews, the objectives of the study were explained to the cattle owners. As the survey was targeted in the rural communities with a very low literacy rate, instead of written consent, we sought verbal consent from the selected study participants. The interviews were conducted during March and April 2017 by visiting each selected household in the village. The Conjoint Faculties Research Ethics Board (CFREB), University of Calgary, Canada and the Research Ethics Boards of Health, Ministry of Health, Royal Government of Bhutan approved the study protocol (Approval number REB16-1945 and REBH/Approval/2017/004, respectively). The questionnaires were checked for completeness before entering the data into Epi Info version 7. 2. 1. 0 [13]. As the data were collected through face-to-face interview by trained survey enumerators, there were only few missing data points and these were identified as “missing data” in the descriptive analysis. The method described by Tack et al. , [14] was adapted to categorize participants as either having an ‘adequate knowledge’ or an ‘inadequate knowledge’ about rabies. Participants were scored on five questions to assess their knowledge about rabies (S1 Table). It was assumed that the participants with adequate knowledge about rabies would be aware of notable clinical signs in a rabid dog, appropriate health-seeking behaviour upon exposure, the health outcome of contracting rabies in humans, a potential rabies reservoir, and at least one mode of rabies transmission. For identifying a rabid dog, irrespective of what other signs participants reported, if any of the five clinical signs listed in the questionnaire (salivation, aggressiveness, biting, aimless movement, and paralysis and death) was mentioned, the participants were considered being able to identify a rabid dog. Since identifying a rabid dog, seeking proper health care after exposure, and knowing the health outcome in humans suffering from rabies is crucial in preventing human deaths due to rabies, participants had to answer these questions correctly. If any of these questions were answered incorrectly, or if participants were not sure of the answer, irrespective of the total score obtained, they were categorized as not having adequate knowledge about rabies. Therefore, a participant with an adequate knowledge would score a minimum of five points, three from the questions on rabies signs in dogs, disease outcome and response upon exposure and two from the questions regarding rabies reservoir and modes of rabies transmission. The method of assessing participants’ attitude was adapted from Dhimal et al. , [15]. Seven questions were used to assess participants’ attitude towards rabies prevention in humans and animals (S2 Table). Participants could choose an answer on a qualitative scale of very low to very high for each question. If the response was “High” and “Very High” participants were awarded one point while for the rest of the responses “Very low”, “Low” and “Medium” no points were awarded. From seven questions, a participant could secure maximum of seven points. Participants were then categorized as having a favourable attitude or an unfavorable attitude based on 80% of the total score as the cut-off, as described by Dhimal et al. , [15]. The data entered into Epi Info database were screened and prepared for analysis in Microsoft Excel 2013 (Microsoft excel 2013, Redmond, USA). Analyses were conducted using R packages “dplyr”, “descr”, “forcats” “lmtest”, “LogisticDx”, “ggplot2” and “stringr” within R statistical software [16–23]. For analysis, the variable age was categorized as 18–35,36–53 and >53 years and the variable education as ‘educated’ or ‘uneducated. Descriptive analysis was conducted for the entire dataset. The frequencies of the categorical socio-demographic variables between the two study areas were compared using Pearson’s chi-square test. The mean age of the participants in the two study areas was compared using student’s t-test. To assess the association between the socio-demographic variables and the binary outcome variables, 1) participants’ knowledge about rabies (adequate vs inadequate) and 2) participants’ attitude towards rabies control and prevention programs (favourable vs unfavourable), a series of univariable logistic regression analysis were carried out. Variables with p-value (≤ 0. 2) were selected for multivariable logistic regression analysis. A forward stepwise method of multivariable logistic regression analysis was performed by adding foremost the variable that had the smallest p-value in the univariable analyses. Subsequently, each of the remaining variable was added. The variables with p≤0. 05 were retained in the final model. The fit of the final multivariable logistic regression model was assessed by conducting Hosmer and Lemeshow test [11]. The odds ratio (OR) and its 95% confidence interval (CI) of the variables associated with the outcome variables were derived from the final multivariable logistic regression model. Confounding was assessed by adding the variables that were not included in the final model as described by Lindahl et al. (24). If the coefficients of the significant variables changed by more than 25%, the added variable was considered to be a confounder. No confounders were observed in our analyses.
  Five hundred and sixty-two participants, 281 each from the south and the east, were interviewed. The response rate was 100%. There was no significant difference (p = 0. 17) between the mean age of participants in the south (45. 8 years) and in the east (47. 5 years). The Chi-square analysis showed that the number of female participants (p<0. 001), participants having children going to school (p<0. 01), participants owning only exotic breeds of cattle (p<0. 001), and owning less than 4 cattle (p<0. 001) were significantly higher in the eastern study areas. The detail of the socio-demographic characteristics in the two study areas is presented in Table 1. Overall, 494 of the 562 (88%) participants had heard of rabies (Fig 2A). In the south, 251 (89%) participants had heard of rabies whereas, in the east, 243 (86%) participants had heard of rabies. Having heard about rabies was not associated with the place of residence. Among the participants who had heard of rabies, 106 (22%) participants did not know the signs shown by a rabid dog while 223 (45%) reported that they would not be able to identify rabies in cattle. While the participants in the east were less likely to know the clinical signs of rabies in dogs (p<0. 001), there was no significant difference in the percentage of participants between the two study areas who could not identify rabid cattle (107 (43%) in the south and 116 (48%) in the east). A total of 288 (58%) participants who had heard of rabies had seen a rabies case, either in a dog, a human or in livestock. The place of residence was not associated with seeing a rabies case. In the south, 155 (62%) participants had seen a rabies case while 133 (55%) participants in the east had seen a rabies case (Fig 2B). The number of participants who knew about preventive rabies vaccination in dogs was 446 (90. 3%). The observation was not statistically associated with the place of residence (224 (89%) in the south and 222 (91%) in the east). In total, 370 (75%, n = 492, two missing) participants were not aware of pre-exposure prophylactic vaccination (PrEP) in cattle. One-hundred and fifty-seven (63%, n = 250, one missing) participants in the south and 213 (88%, n = 240, one missing) participants in the east reported not knowing about PrEP in cattle. Furthermore, 334 (68%, n = 493) participants reported not knowing about the PrEP option for humans. In total 441 (89%) participants reported that rabies can be effectively prevented in humans after a potential exposure. However, only 399 (81%) participants knew about the standard PEP regimen which consists of washing the bite wound with soap and water followed by injection of four to five doses of rabies vaccine. Of the remainder, washing the bite wound with soap and water as standard PEP regimen was reported by 16 (3%) participants, washing the bite wound and a shot of vaccine by 32 (7%), and 47 (9%) reported not knowing about the regimen. The proportion of individuals aware of the standard PEP regimen was higher in the southern study group than the eastern study group (p<0. 0001). Among the participants who had heard of rabies, 195 (39%) participants had adequate knowledge about rabies (Fig 3A). The multivariable regression analysis demonstrated that individuals residing in the south were 9. 25 times more likely to have adequate knowledge about rabies than their counterparts in the east [OR = 9. 25 (95% CI: 6. 01–14. 53) ], while the individuals who had seen a rabies case were 2. 5 times more likely to have adequate knowledge about rabies than those who had not seen a rabies case [OR = 2. 46 (95% CI: 1. 6–3. 82) ] (Table 2). Based on our scoring criteria, 323 (65%) of the total study participants who had heard of rabies had a favorable attitude towards rabies control and prevention programs (Fig 3B). In the south, 144 (57%) participants had a favorable attitude while 179 (73. 7%) in the east. The multivariable logistic regression analysis showed that an individual residing in the east was 2. 08 times more likely to have a favorable attitude than a person residing in the south [OR = 2. 08 (95% CI: 1. 43–3. 05) ] (Table 3). Only 81 (14%) participants reported stall feeding their cattle (South 79 (28%); east 2 (1%) ) while 155 (28%) reported practicing extensive grazing, 174 (31%) semi-extensive grazing and 148 (26%) tethering cattle. Of the 555 participants (7 missing), 143 (26%) reported not having a shed for their cattle while 240 (43%) reported having a temporary shed. Only 172 (31%) participants reported having reliable cattle shed with concrete flooring and appropriate roofing. The number of participants having reliable cattle shed was more in the south compared to the east (108 (39%) and 64 (23%), respectively. Five-hundred and seventeen participants (92%) stated that they would either report a cow that had died of illness to a livestock official or they would bury the carcass. Of these, 427 (76%) participants reported that they would bury the carcass while 90 (16%) would report to a livestock official. However, 15 (3%) participants reported dressing the carcass to sell the meat, 15 (3%) reported dressing carcass for family consumption, and 15 (3%) reported selling the whole carcass. In total, 490 (87%) participants reported assisting their cattle during parturition, 512 (91%) reported handling sick cattle, 404 (72%) reported examining oral cavity, 471 (84%) reported dressing wounds in animals, and 138 (25%) reported dressing carcasses. The proportion of participants who dressed cattle carcasses was twice as much in the east than the south (33 and 16% respectively). Among the participants who reported engaging in the mentioned activities, 25 (18%) reported using minimal personal protective equipment (PPE) while dressing carcass (15 in the south and 10 in the east). Similarly, 121 (26%) reported using PPE while dressing a wound in their cattle, 114 (23%) while assisting parturition, 88 (22%) while examining oral cavity, and 127 (25%) while handling sick animals. However, in both the study areas, more than 95% of the participants reported washing their hands after engaging in on-farm activities. Three-hundred and fifteen participants (64%) reported the neighbor as the most common source of rabies information followed by formal news media such as television, radio, and newspaper (122 (23%) ). One hundred and thirteen (22%) participants reported hearing about rabies from animal health training programs and rabies awareness campaigns, 58 (12%) from family members, 45 (10%) from school going children, and 8 (2%) through internet (Fig 4) This study has shown that there is a lack of comprehensive knowledge about rabies, especially regarding the modes of transmissions, identifying rabid animals (dogs and cattle), the severity of the outcome of rabies infection in humans, and the recommended PEP regimen, in both the study areas. Therefore, future rabies education programs should focus on educating communities on the severity of the outcome of rabies infection in humans and animals, modes of transmission, appropriate health-seeking behaviours after a potential exposure, and good farm practices. It is also essential to include topics such as the importance of responsible animal (dogs and livestock) ownership and community participation in rabies control programs. The observation that participants in the eastern rabies low-risk areas have less knowledge about rabies compared to the participants in the areas within the rabies high-risk zone underlines the need to extend rabies education programs to the communities close to the borders and other areas where rabies incursions are more likely.
summary: The impacts of rabies outbreaks in cattle and other livestock are multifold. At the local level, economic losses resulting from the direct loss of cattle and the animal’s future productivity is a significant threat to the livelihoods of subsistence farming communities. Besides, rabies in livestock poses a potential public health threat associated with human exposures that result during handling sick animals and dressing carcasses of animals that had died of rabies. Furthermore, the Government incurs costs for responding to outbreaks and providing post-exposure prophylaxis (PEP) to potentially exposed individuals. We conducted a KAP questionnaire surveys among cattle owners in two selected study areas of Bhutan to understand the level of rabies awareness among the cattle owners, their attitude towards rabies prevention and control and to identify existing on-farm practices that can result in potential exposure to rabies in animals and humans. We observed that there was a lack of comprehensive knowledge about rabies especially regarding the post exposure care and outcome of rabies infection in humans and animals. Given that most participants lacked knowledge about clinical signs of rabies in cattle their engagement in practices such as examining oral cavity, assisting cattle during parturition and dressing wounds without wearing minimal protective equipment, was concerning. Our study identifies the need to extend rabies education into the rural communities of Bhutan. Furthermore, our findings reiterate the importance of rabies education as a crucial component of the global initiative to eliminate dog-mediated rabies in humans and animals.
keywords: livestock
  bhutan
  medicine and health sciences
  health education and awareness
  statistics
  immunology
  tropical diseases
  geographical locations
  vertebrates
  animals
  mammals
  dogs
  health care
  regression analysis
  preventive medicine
  rabies
  mathematics
  neglected tropical diseases
  vaccination and immunization
  veterinary science
  research and analysis methods
  public and occupational health
  infectious diseases
  veterinary diseases
  zoonoses
  mathematical and statistical techniques
  agriculture
  people and places
  eukaryota
  asia
  biology and life sciences
  viral diseases
  physical sciences
  amniotes
  statistical methods
  organisms
title: A community-based knowledge, attitude, and practice survey on rabies among cattle owners in selected areas of Bhutan