Assessment of Biosecurity Status in Commercial Chicken Farms Found in Bishoftu Town, Oromia Regional State, Ethiopia

A survey was undertaken from December 2017 to April 2018 to assess the biosecurity status of 44 commercial chicken farms established in Bishoftu town, Ethiopia, by interviewing farm owners using a structured questionnaire. The obtained data were summarized using frequency tables and analyzed with Pearson's chi-square test and Fischer's exact value using Stata 14 statistical software. From the assessed chicken farms, 31 (70.45%) were located within 0–50 m from the main road, 39 (88.64%) situated 500 m from the nearest farms, and 27 (61.36%) placed within 0–20 m from the residential areas. Forty-one (93.18%) participants disclosed that their employees did not receive training on biosecurity. From the assessed chicken farms, 30 (68.18%) had fences, 40 (90.91%) had footbaths at their gates, 31 (70.45%) prohibited visitors entrance, and 39 (88.64%) did not exchange equipment with other farms. In addition, 26 (59.09%) farms were easily accessed by wild birds, each of 42 (95.45%) farms purchased day-old chicks and feed, and 40 (90.91%) shared trucks with other farms as well. Among the assessed farms, only 2 (4.55%) had signages to restrict people's access, 9 (20.45%) had isolation rooms for diseased chickens, 14 (31.82%) disposed of dead birds properly, and 10 (22.73%) kept various types of records. Occupation (Fischer's exact value = 8.40; P=0.019), previous training (Fischer's exact value = 4.40; P=0.044), source of the premises (χ2 = 5.50; P=0.019), and farm capacity (Fischer's exact value = 13.50; P=0.002) were found statistically significantly associated with the farm biosecurity status. The farm biosecurity status was found to be good in farms that were run by civil servants, had trained employees, are owned premises, and were of large and medium scales. In conclusion, the higher poor biosecurity status on chicken farms calls for the implementation of good biosecurity practices in each farm as well as the provision of training to the farm owners and their employees.


Introduction
Poultry production is a very important type of animal production [1]. Poultry are efficient in producing highquality protein (meat and eggs) [2]. However, poultry diseases remain the principal causes of failure in poultry production [3]. A successful animal production, including poultry, requires the adoption of good biosecurity practices [4], which is the most effective and inexpensive disease control measure [5]. Biosecurity in the poultry refers to a set of practices and measures taken to limit, control, or prevent the introduction and dissemination of infectious diseases in the poultry premises and facilities [6,7]. A biosecurity program uses a combination of physical barriers such as fences, mesh wire, and directed actions to prevent the introduction of or minimize the spread of infectious diseasecausing agents including the use of footbaths, carwash deep, and disinfection of farm equipment [2]. e three components of biosecurity measures are isolation, traffic control, and sanitation [8]. Van Limbergen et al. [4] and Sasaki et al. [9] disclosed that biosecurity is classified into internal and external. Biosecurity consists of conceptual, structural, and operational frameworks [10]. e conceptual category includes: the location of farms; structural: covering the building design and facilities to protect against entry of wild birds and predators; and operational: covering the routine disinfection, sanitation, and work procedures those farm employees and visitors follow [11]. e performance of birds is influenced by the biosecurity measures of the farms [5].
Ethiopia has an estimated poultry population of about 56.53 million [12]. e poultry production is characterized by small scavenging flocks of local chicken and few farms in the commercial subsector with varying flock sizes [13]. e small-and medium-scale producers constitute most of the commercial poultry production in Ethiopia [14]. So far, there have been very few attempts on the assessment of biosecurity measures of commercial poultry farms [15,16] and poultry markets [17] of Ethiopia. Haftom et al. [15] reported that out of 25 small-scale poultry farms, 12 (44%) did not employ all-in all-out practice, 14 (56%) disposed of dead birds by throwing, and 16 (64%) kept different age groups together. e existing evidences depicted failure to fully practicing biosecurity measures in the integrated and larger commercial-scale types while virtually no or minimal routine application of biosecurity measures in the small-scale poultry production system [18].
Poultry production is important in Ethiopia as poultry play a major role in poverty alleviation, nutrition, and food security [14]. In Ethiopia, the chicken production system is classified into small-, medium-, large-, and integrated large commercial-scale production systems [18]. Ethiopia has small-, medium-, and large-scale intensive broiler and layer farms located in and around Addis Ababa, Debre Zeit (the now Bishoftu), Modjo, and Adama [19,20]. Most small-scale poultry farms are located around Debre Zeit town in the Oromia region and Addis Ababa. e main commercial poultry farms, including Elflora, Agro Industry, Genesis, and Alema, are located around Debre Zeit in Oromia [19].
In Ethiopia, the application of biosecurity measures is limited [19], and to date, there is no information on the biosecurity status of commercial chicken farms in Bishoftu town. erefore, the objective of this study was to assess the biosecurity practices of commercial chicken farms and identify the predictors of good biosecurity status in commercial chicken farms in Bishoftu.

Study Area.
is study was carried out at Bishoftu town, East Shewa Zone of Oromia regional state. It is located 45 kilometers southeast of Addis Ababa, at 9°N latitude and 40°E longitude (Figure 1). Bishoftu town is located at an altitude of 1850 meters above sea level in the central high land of Ethiopia [21]. Farmers in the vicinity of Bishoftu use a mixed crop and livestock farming system. Moreover, Bishoftu and its surroundings have variable and yet representative agroecologies of the country. ese agroclimatic zones are inhabited by different plant and animal species [22].

Study Population.
e target population of the study comprised 50 commercial chicken farms at Bishoftu town that raise exotic breeds of chickens (predominantly Bovans and Lowmans) on a small scale (<1000 birds), medium scale (1000-10,000 birds), and large scale (>10,000 birds) [19]. ese exotic chicken breeds are imported and are highly productive than the indigenous breeds of chicken.

Study Design and Sampling Technique.
A cross-sectional population survey was carried out from December 2017 to April 2018 to evaluate the biosecurity status adopted by commercial chicken farms at Bishoftu town. e list of commercial chicken farms was obtained from the Ada'a Woreda Livestock and Fisheries Development Office. ese farms were visited in person during data collection, and the owners were contacted and asked for their interest to participate in the biosecurity study. Verbal consent for participation was obtained only from 44 farms, while others refused to participate, and the reasons for refusal were not sought.
e survey comprised face-to-face interviews of farm owners using a structured questionnaire. e interview was carried out by the same person.

Questionnaire Development.
A structured questionnaire was developed and used to collect data on the biosecurity adopted by small-, medium-, and large-scale commercial chicken farms at Bishoftu. For the survey, owners' demography, farm characteristics, and relevant biosecurity practices were included in the questionnaire. Specific questions included were the demography of commercial chicken farm owners (gender, occupation, education level, experience in running chicken farms, and training received) and characteristics of the farms (premises, farm capacity, and farm type). Questions associated with the biosecurity  assessment consisted of the conceptual framework such as distance from the main road, between farms, and from the residential area; presence of standing water; house type; housing position; and material used for house construction. In the structural framework, questions included were the presence of farm fence and gate, footbath, prohibition of vehicle entry, presence of tire bath/spray, prohibition of visitors, visitors sign-on logbook, no purchase of day-old chicken, no purchase of feed, no sharing of the truck with other farms, permanent rodent control, no access to stored fresh litter for wild birds, and presence of permanent wild bird control. At last, questions included in the operational biosecurity framework were the use of special cloth, footwear, masker, and hat; regular cleaning and disinfection; use of high-pressure sprayer; proper disposal of dead chicken; no other animals on the farm; veterinary consultation; inbetween disinfection cycle; prophylactic treatment and vaccination; and so on. In general, a total of 69 closed questions were designed to obtain "yes" or "no" answers.

Data Collection.
e questionnaire was pretested in ten chicken farms that were included in the survey, and care has been taken to avoid any misunderstanding or misinterpretation of the questions. e personal face-to-face interview was made to farm owners, managers, veterinarians, and employees. In addition, the farms were observed to assess the level of biosecurity at different levels.
2.6. Data Analysis. All collected data were entered into a Microsoft Excel spreadsheet, cleaned, and coded. Variables that are assumed to have a similar influence on the potential risk of introduction of contagious disease on the farm combined into a single variable, by producing a basic biosecurity score as a method described previously by [24]. e minimum and maximum biosecurity score obtainable on a farm were 0 and 72, respectively. e total sum assigned to the farm was divided by the maximum score that the farm could attain with the questions actually answered (72) and multiplying this proportion by 100 to obtain the percentage. A farm that gained >50% was considered having "good biosecurity practice", and <50% as "poor biosecurity practice". Statistical analyses were performed using STATA, version 13 statistical software. Pearson's chi-square or Fisher's exact test was used to estimate associations between demography of chicken farm owners and farm characteristics with the biosecurity status. A variable is said to have a significant effect when P < 0.05.

Demography of Farm Owners.
Of the 44 commercial chicken farm owners, 28 (63.64%) were males; 26 (59.09%) had higher education in various fields; 30 (68.18%) were traders; and 31 (70.45%) had previous experience in rearing chickens. Among those owners, 12 (27.27%) refused to disclose their level of education, and 20 (45.45%) did not receive training on chicken farm management. e demography of chicken farm owners is presented in Table 1. Table 2, 32 (72.73%) were run on a rented premise, while only 12 (27.27%) were established on owned premises. e majority (86.36%) were categorized as small-scale chicken farms, and in 28 (63.64%) of them, only layers were reared.

Biosecurity Evaluation
3.3.1. Conceptual Biosecurity. A total of eight biosecurity indicators were used to assess the concept of biosecurity and summarization revealed a mean score of 3.3 points with a standard deviation (SD) of 1.76. Among the 44 Bishoftu chicken farms, 31 (70.45%) were located within 0-50 m from the main road and 39 (88.64%) farms were established within 500 m from the nearest farm (Table 3). Furthermore, 27 (61.36%) were situated within 0-20 m from the residential area, and 10 (22.73%) were placed within 21-200 m. All (100%) the premises constructed for chickens were modified open sided with curtains, and 10 (22.73%) of them were built in the east-west direction. e employees of 41 (93.18%) farms disclosed that they did not receive any training on application biosecurity measures.

Assessment of Association between Biosecurity Level and Owners' Demography and Farm
From 24 farms whose owners received training, 9 (37.5) graded "good", while 32 out of 38 small-scale and all broiler (n � 11) type chicken farms graded "poor". Around 84.4% (27/32) of farms established on rented premises had poor biosecurity status. However, the association between owners' gender, education level,     experience, and biosecurity status were statistically insignificant (P > 0.05; Table 6).

Discussion
is survey provides baseline information on the demography of people owning chicken farms and an insight into the biosecurity practices performed among the chicken farms established in Bishoftu town. However, limitations of this study were failure to assess the routine application and functionality and overlook the relative importance of each indicator to the overall biosecurity measures. e majority of farm owners were males, completed higher education, and experienced in chicken rearing. Likewise, Ajewole and Akinwumi [25] and Kouam et al. [8] disclosed that the majority of small-scale broiler farmers were men. Kouam et al. [8] explained that this age-wise variation was attributed to the requirement of high commitment for success.
Although the majority of owners in this study had higher education, many did not receive training on biosecurity. Kouam et al. [8] linked this with the negligence of government officials to provide training in biosecurity as they lack understanding of the usefulness of biosecurity in animal husbandry, and this might also be partly the case in Bishoftu. e majority of the chicken farms in Bishoftu town were small-scale farms with <5,000 birds rearing only layers on rented premises. In Egypt, 60% of broiler chicken farms were also small scale [6]. Many commercial chicken farms at Bishoftu were located near the main roads (<0-50 m) and in close proximity (<500 m). ese present danger of airborne transmission of diseases from animals transported along the public road and between poultry farms. us, to minimize such transmission, the distance to the nearest poultry farm should be at least 500 m and preferably >1 km [26]. Several chicken farms at Bishoftu were located within 0-20 m from the residential area. is poses a biosecurity risk and considerable economic loss to the chicken farms as well as   6 Veterinary Medicine International animal and public health problems through water/soil and air pollution [27].
In the present study, 30 out of 44 farms did not dispose of carcasses of dead chicken properly, and 27 out of 44 did not store removed litter at cover shade. However, carcasses of dead chicken and used litter must be disposed of properly because they are rich sources of infectious agents [4,5]. Disposal of litter by spreading on nearby arable farmlands constitutes a risk of dissemination of disease-causing organisms [28]. us, those farms are at risk of the spread of infectious agents.
In this study, many farms were located far from standing water, and this finding varies from that of Kouam et al. [8] who reported that 73.5% of farms were located less than 500 m from a stream that poses a risk of pathogen transmission among poultry as water spots such as ponds, lakes, and rivers are attractive to migratory birds [29]. With regard to structural biosecurity, nearly all farms in this study had footbath at the gate, and this was higher than the finding of [30,31] who reported 80% of the farms in Mekelle had footbath at the farm gate and only a small number of respondents set up a footbath at the farm entrance (37% from broiler farms and 18% from the layer farm). is difference may be due to better awareness of farm owners about disease spread by shoes of visitors and farmworkers. However, only a few poultry farms prohibited vehicle entry and apply tire spray/bath that poses a great risk as these trucks can spread a pathogenic microorganism onto the farm. Vehicle movement between farms is associated with farm infection [32]. e current study revealed that almost all farms purchase replacement chicken. is finding is higher than that of [33] who disclosed that 63.6% (7/11) of farmers sourced their birds from distributors without knowing the hatchery. Besides, the possibility of infection at the hatchery, day-old chicks may also be carriers of vertically transmitted (from hen to chick) pathogens such as Mycoplasma spp. [29]. is posed a substantial risk for poultry farms; even though the farm implements biosecurity measures upon the introduction of day-old chicken from other farms, the probability of pathogen entering the farm is high.
is is because each poultry farm has its own risk profile for the introduction of pathogens, disease development, and spread of pathogens to other poultry farms [34]. Several studies have already pointed out that buying animals from different farms entails a greater risk of the introduction of disease-causing agents [35].
Many poultry farms at Bishoftu were prohibiting visitor's entry. is finding was in line with the study conducted in Egypt by Mohammed and Helal [36] who found 28.6% of small commercial poultry producers allowed visitors to enter poultry shades. But this finding disagrees with the finding of Birhanu et al. [31] who reported 76% of farms allowed visitors entry. e higher prohibition of visitors entrance observed in this study may be attributed to commercial poultry producers in Bishoftu town who have a better awareness of the risk of allowing visitors onto farms than those in Mekelle. Human movement among farms was shown to be an important risk factor for poultry diseases such as avian influenza [28] that is encouraging as visitors could access different farms and thereby introducing pathogens onto farms. To limit the risk of human movement, an entrance to a farm should be limited to one [37], and visitors should sign on a logbook when visiting a farm to enable rapid identification of people and farms during an outbreak [38]. Almost all of the farms involved in the present study bought feed from different sources that present the risk of introducing pathogens onto the farms. Besides lorries that can act as a mechanical vector, the feed can also be a source of infection. e feed can be contaminated with, for example, Salmonella spp., Escherichia coli, Clostridium spp., Aspergillus spp., and mycotoxins. e contamination of the feed can occur at different times during the production, storage, or transport [29].
From the surveyed farms only, a few farms implemented permanent rodent control, and wild birds were denied access to poultry houses. Failure to implement this practice constitutes a biosecurity risk as wild birds and rodents are carriers of pathogenic microorganisms that substantially affect the commercial poultry producers; especially, migratory wild birds are the cause of transboundary disease transmission. is finding was not in line with the study conducted in Khartoum that revealed that 33 (73.3%) of the farms controlled the entry of wild birds, rodents, or insects into poultry sheds or had strict measures to keep other poultry and domestic animals away from their flock [39]. e presence of reservoir wild birds influences the risk of introduction of poultry diseases such as avian influenza [37,40,41]. To attain biosecurity, rodents' entry must be minimum [5]. In operational BM perspectives, the present survey revealed that in more than half of the farms, regular cleaning and disinfection were undertaken, and this finding was lower from the study performed at Mekelle in which 88% of the farms assessed carry out regular cleaning and disinfection of equipment. Lower levels of biosecurity are associated with a higher prevalence and outbreak of avian disease [4,42].

Conclusion
e findings from this study suggest that the practice of biosecurity implementation in commercial chicken farms at Bishoftu town was poor or lower with few farm owners who had been trained on the importance of proper biosecurity adoption. e majority of the biosecurity risks for chicken farms originated from inappropriate site selection, purchase of replacement day-old chicken and feed sources, and lack of training to farm employees. erefore, there is a need to develop a biosecurity plan and find appropriate ways to educate the farm owners as well as farm employees and convince them to heed the plan.
Data Availability e data are included in the tables within the manuscript.