Epidemiological study of bovine brucellosis in indigenous cattle population in Kibondo and Kakonko Districts, Western Tanzania

G Y Chitupila, E V G Komba¹ and N J Mtui-Malamsha²

Department of Livestock and Fisheries Development, P.O Box 9, Kibondo, Tanzania
ekomba@suanet.ac.tz
¹ Department of Veterinary Medicine and Public Health, Sokoine University of Agriculture, P. O Box 3021, Chuo Kikuu, Morogoro, Tanzania;
² Ministry of Livestock and Fisheries Development, P.O Box 9152, Dar es Salaam, Tanzania

Abstract

A cross-sectional epidemiological study of bovine brucellosis was conducted between December, 2013 and January, 2014 in Kibondo and Kakonko Districts of Kigoma region, Western Tanzania. A total of 410 animals aged ≥6 months from 60 herds were tested for Brucella abortus antibodies using Rose Bengal Plate Test (RBPT) and Competitive-Enzyme–linked immunosorbent assay (c-ELISA) as screening and confirmatory tests, respectively. Sampling process of study units adopted a multistage cluster sampling. Information regarding risk factors influencing Brucella seropositivity, livestock owner’s knowledge, attitudes and practices (KAPs) were gathered using questionnaire administered to 60 livestock keepers.

The overall individual animal brucellosis seroprevalence was 5.6% (95% Confidence Interval [CI]: 3.8-8.3); and herd level seroprevalence was 21.7% (95% CI: 13.1-33.6). Kibondo had animal level seroprevalence of 9.4% (95% CI: 6.1-14.2) and herd level seroprevalence of 30.0% (95% CI: 16.7-47.9), while Kakonko had animal level and herd level seroprevalence of 1.9% (95% CI: 0.8-4.9) and 13.3% (95% CI: 5.3-29.7), respectively. Improper disposal of aborted materials (OR= 6.4; 95% CI: 1.2-33.5; p=0.03), contact with dogs (OR= 7.4; 95% CI: 1.6-31.9; p=0.01) and contact with small ruminants (OR= 8.9; 95% CI: 2.8-55.9; p=0.03) had significant association with seroprevalence of brucellosis. Results revealed low degree of awareness and accurate knowledge of livestock keepers on brucellosis and its zoonotic potential. In the study area bovine brucellosis is prevalent; therefore there is a need to create general public awareness about the disease and design and implement control measures that will prevent further spread of a disease within and outside the study area.

Keywords: Brucella abortus, Kigoma, risk factors, seroprevalence

Introduction

The economy of Tanzania depends largely on agriculture, of which livestock rearing forms an integral part (Ministry of Agriculture and Cooperatives 1995). As the economic future of the country lies mainly in agriculture development, diseases with considerable effect on livestock productivity and human health such as brucellosis should be controlled by all means possible (John et al 2010). Zoonotic diseases like brucellosis remain a serious obstacle to public health, socio-economic progress; and food safety and security in most African countries (OIE 2009).

Brucellosis, caused by bacteria of the genus Brucella, is a contagious infectious disease affecting various species of domestic animals, wildlife, marine mammals as well as humans (Lopes et al 2010; Galinska et al 2013). It is primarily a reproductive disease of animals, characterized by late term abortion, infertility, reduced milk production as a result of retained placenta, endometritis and varying degrees of sterility in bulls and cows (Jergefa et al 2009; Karimuribo et al 2007). Bovine brucellosis is usually caused by B. abortus; a Gram-negative, facultative intracellular coccobacilli bacterium. The disease is less frequently caused by B. melitensis, particularly when cattle are kept in close association with sheep and goats; and occasionally by B. suis (OIE 2009; Dinka et al 2009), which may cause a chronic infection in the mammary glands of cattle but it has not been reported to cause abortion or spread to other animals (Lopes et al 2010). The disease is a major cause of reproductive failure in domestic animals in many parts of the world (Corbel 1988), causing substantial economic losses to livestock keepers as well as a nation at large (Karimuribo et al 2007; Holt et al 2011).

In Sub-Saharan African countries including Tanzania, brucellosis is endemic and widespread although with varying prevalences (Matope et al 2011; Karimuribo et al 2007). In the country the history of the disease dates back to 1927 when an outbreak of abortion was reported in Arusha region and the first laboratory confirmation of the disease was performed in 1928 (Karimuribo et al 2007). Serological surveys carried out in different parts in the country, indicated herd level seroprevalence of 12.2% in Kilimanjaro, 5.3% in Tanga, 3.2%-4.2% in Manyara region, 15% and 10.8% in Mwanza (1962 and 1996), 15.2% in Arusha, 3.3% and 7.6% in Mbulu and Masailands, 5.2% in Dodoma, , 12.0%-14.0% in Dar es Salaam and 13.2% in Iringa (Karimuribo et al (2007) and Swai et al (2010). In Western Tanzania, including Kigoma region, the disease has been insufficiently investigated and to date there is no published data on its status, magnitude and distribution. Similarly assessment of risk factors influencing Brucella seropositivity, livestock keeper’s awareness, knowledge, attitude and practices regarding brucellosis has also not been conducted. It was therefore, the aim of this study to establish seroprevalence of bovine brucellosis; identify risk factors influencing Brucella seropositivity; and assess livestock owner’s knowledge, attitude and practices (KAPs) regarding brucellosis. The generated information will contribute to data that may be used to device appropriate local and national strategies for the control of the disease.

Materials and methods

Study area and animals

This study was conducted in Kibondo and Kakonko Districts, Kigoma Region. The Districts are located in the Western Plateau of Tanzania and they lie between Lat 3.9° –5.0° S, and Longt 30.2° –31.5° E with an average altitude that ranges between 500 m and 2300 m above the sea level. Temperature ranges between 15°C and 22°C; while rainfall ranges between 800 mm and 1900 mm. Humidity ranges between 30.0% and 45.0% depending on the season.

Kibondo District has 10,572 indigenous cattle and 140 cross bred dairy cattle while Kakonko District is estimated to have 20,938 indigenous cattle and 485 cross bred dairy cattle (Kibondo Local government monitoring data base 2 of 2013-2014; LGMD2). The predominant farming system in both Districts is mixed crop–livestock farming, where animals are kept under extensive traditional grazing management systems which enable animals from different herds to mingle in communal grazing areas and watering points. In this study, a herd was also regarded as a cluster and was defined as a group of cattle (of both sexes) kept in one enclosure and constituting ten or more animals aging six months and above. Furthermore, herds were classified into two categories; large herds (> 15 animals) and small herds (≥10≤ 15 animals) basing on the classification used by the departments of Livestock and Fisheries Development in the study area. Cattle aging >2 years were representing adults and those aging ≥0.6 ≤2 years were representing young animals adopting categorization of age groups used by Degefu et al (2011).

Study design and sample size calculations

A cross-sectional study was carried out from December, 2013 to January, 2014. The sample size of animals was determined using the formula n=1.96²P (1-P)/d² (Naing et al 1996) using expected prevalence (P) of 0.20, precision level (d) of 0.05 and confidence level of 95% which resulted in required sample size of 245 animals. Since multistage cluster sampling technique was used, in order to achieve the same precision, the original sample size was multiplied by the design effect (D) calculated using the formula D=1 + (b-1) roh (Otte et al1997). The average number of samples per cluster (b) was 7 and intra-cluster correlation coefficient or rate of homogeneity (roh) was 0.10. Number of clusters (c) sampled was determined by the formula c=P (1-P) D/SE²n and Standard error (SE) was calculated by SE=d/1.96 (Otte et al 1997). Accordingly, the total number of animals to be bled was 392 and the number of clusters to be sampled was 56. But ultimately 410 animals that are; 202 and 208 animals were sampled from Kibondo and Kakonko Districts, respectively. These were obtained from 60 clusters (30 per district and 3 per village) picked from 20 villages (10 per district). Selection of study herds (which resulted in the recruitment of households) and villages was done by a simple random sampling technique after developing a list of all villages keeping cattle (40 and 32 villages from Kibondo and Kakonko Districts respectively) and eligible herds for each district. Individual animals in the herd were selected by a systematic random sampling technique.

Data collection

1. Blood sampling

To establish seroprevalence, about 5ml of blood sample were collected from the jugular vein of each animal using plain vacutainer tube and needles (Zhejing Kangshi Medical Device Co., Ltd, China). Each sample was labelled by using codes describing the specific animal and herd. The samples were left to clot at room temperature overnight and subsequently centrifuged at 3000 rpm for 10 minutes to obtain clear serum. About 2 ml of serum was collected into cryovials and stored at -20°C in Kibondo District Hospital until serological analysis was performed (a month later) at the Faculty of Veterinary Medicine laboratories, Sokoine University of Agriculture.

2. Laboratory analysis of sera samples

All collected sera samples were first screened using Rose Bengal Plate Test (RBPT) for Brucella antibodies according to the test procedure recommended by OIE (OIE 2009). Briefly, 30µl of RBPT antigen and 30µl of the test serum were placed alongside on the glass plate and mixed thoroughly. After 4 minutes of rocking, any visible agglutination was considered as positive result. RBPT positive sera were then subjected to competitive enzyme linked immunosorbent assay (c-ELISA) as confirmatory test, adopting a test procedure and interpretation of results as recommended by the manufacturer (Animal Health and Veterinary Laboratories Agency-AHVLA, New Haw, Addlestone, Surrey, KT153NB, UK). Only animals positive on c-ELISA were regarded as Brucella seropositive. A herd was considered positive for the disease when at least a single animal tested positive for c-ELISA.

3. Questionnaire survey

A structured questionnaire was administered to 60 livestock keepers in 60 households (30 per district) where blood samples from animals were collected. The questionnaire was pretested in the field and adjusted as required. Interview was conducted to a member of the household who was more conversant about the herd using Swahili dialect by trained Livestock Field Officers in the study area. Data on risk factors for Brucella seropositivity, livestock owner’s knowledge, attitudes and practices regarding brucellosis were collected. Information on individual animal variables (age, sex, previous history of abortion) was recorded separately on sample data sheets.

Statistical data Analysis

Data were first entered and cleaned in Microsoft Excel and imported into STATA version 12 (Stata corp, College Station, TX, USA) for analysis. Descriptive statistics, particularly frequencies were computed for proportions of positive animals and herds. The association between individual animal and herd level factors and brucellosis seroprevalence was investigated in two steps using logistic regression. In the first step, relationships between each explanatory and outcome variable was individually investigated in univariate analysis. The predictor variables were assessed for collinearity using Pearson’s Chi-square test. Only variables with p-values < 0.20 in univariate analysis were included in second step (Multivariate model). The model was constructed by a forward stepwise selection of variables utilizing likelihood ratio test p values. Variables were retained in the model if likelihood ratio test p values were ≤ 0.05. The model was evaluated for goodness- of- fit using a Hosmer-Lemeshow test. The potential confounding effect of those variables not retained in the final model was assessed using Mantel-Haenszel Chi-Squared test. A variable was considered a confounder if it resulted in > 20.0% change in the odds ratio. The discrimination ability of final model was assessed using the receiver operating characteristics (ROC) defined as the area under the curve (AUC). The interaction term was introduced in the final model to assess effect of modification. For final analyses, a p-value of ≤ 0.05 was taken as significant. The calculated seroprevalences and comparisons thereof were based on c-ELISA results.

Results

The seroprevalence of brucellosis

The overall seroprevalence of brucellosis at animal level was 5.6% (95% CI: 3.8-8.3) while at herd level it was 21.7% (95% CI: 13.1-33.6). The seroprevalences for individual Districts are as indicated in tables1 and 2. At animal level Kibondo District had a significantly higher prevalence (9.4%; 95% CI: 6.1-14.2) than Kakonko district (1.9%; 95% CI: 0.8-4.8) (p=0.002). At herd level, however, the seroprevalence in Kibondo District (30.0%; 95% CI: 16.7-47.9) and that in Kakonko District (13.3%; 95% CI: 5.3-29.7) didn’t show statistically significant difference (p=0.21). The overall seroprevalence of brucellosis in female animals was 6.6% (95% CI: 4.3-9.8) while in male animals it was 2.2% (95% CI: 0.7-7.7) as indicated in table 3. Table 3 also presents seroprevalences of brucellosis between the two sexes at individual District level. The differences in overall and District level seroprevalences between the two sexes were not statistically significant. No exposure to Brucella was observed in young animals based on c-ELISA results where as in adult animals an overall seropositivity of 7.6% (95% CI: 5.2-11.2) was recorded and the difference between the two age groups was statistically significant (p=0.01) as seen in table 4 which also displays age specific seroprevalences of brucellosis for individual Districts. The seroprevalences of brucellosis in large herds and in small herds are presented in table 5. No statistically significant differences in seroprevalences between small and large herds were noted at both the overall and individual District levels.

Factors affecting the overall seroprevalence of bovine brucellosis

Univariate analysis indicated that; contact with pigs, small ruminants, wildlife, sourcing replacement animals from livestock market, improper disposal of aborted materials, use of bulls from other herds and use of dogs as guardians during grazing qualified for multivariate analysis (p<0.20), while sourcing replacement animals in the village, sourcing replacement animals from outside the village, use of own bull for breeding, irregular cleaning of a boma, absence of parturition pen, contact with other animals at watering points and contact with other animals during grazing could not qualify for multivariate analysis (p>0.20). Multivariate analysis revealed that; contact with small ruminants (p=0.03), improper disposal of aborted materials (p=0.03) and use of dogs as guardians during grazing (p=0.01) had a significant effect on the overall seroprevalence of bovine brucellosis in the study area (Table 6). There was no evidence of collinearity of predictor variables. Similarly no significant interactions and evidence of confounding were detected. The Hosmer-Lemeshow test showed that the model fit the data (X2 =1.37, d.f. =2, p=0.50). The ROC defined as AUC (0.82) suggested that, the final model had good discrimination ability.

Livestock owner’s knowledge, attitudes and practices (KAPs) regarding brucellosis

Results on assessment of knowledge, attitudes and practices regarding brucellosis are presented in table 7. A small proportion of the respondents was aware of brucellosis and had seen suspected cases of the disease in animals. They mentioned abortion, infertility, intermittent fever and weak newborns as signs of the disease in animals. Information contained in the table also indicates existence, among farmers, of attitudes and practices linked to the spread and persistence the disease in the study area.

Discussion

Seroprevalence

The results of this study indicate that, bovine brucellosis is prevalent in Kibondo and Kakonko Districts of Kigoma Region. The overall animal level seroprevalence (5.6%) obtained was lower than those reported earlier both in the country (Karimuribo et al 2007, 6.2%; Swai et al 2010, 7.3%) and in Zambia (Muma et al 2013, 20.7%). Seroprevalence levels lower than the one reported in the current study have been estimated elsewhere in Ethiopia (Mergesa et al 2011, 3.5%; Berhe et al 2007, 3.2%). The two investigations however reported slightly higher herd level seroprevalences of 26.1% and 42.3% respectively. Swai et al (2010) reported a slightly lower (20.0%) herd level seroprevalence than what is reported in this study. According to FAO (2002); in Africa basing on RBPT test, high prevalences (> 20.0%) were reported in Rwanda and Togo; moderate prevalences (10.0% - 20.0%) were reported in Mali, Uganda and Senegal; while low prevalences (< 10.0%) were encountered in Benin, Ethiopia and Ghana. The variations in prevalence which were observed between reports and countries could be attributed to several factors including differences in types of livestock management systems, laboratory techniques used in diagnosis of the disease and study designs adopted in different investigations.

The present study has revealed higher seroprevalence of bovine brucellosis in Kibondo district than Kakonko district both at individual animal and herd levels, the former being statistically significant (p<0.05). The observed significant difference in animal level seroprevalence between the two Districts requires a further well designed study to capture all the possible contributors to such a difference.

In this study, a slightly higher prevalence (6.6%) of brucellosis was estimated in female animals as compared to male animals (2.2%) but this difference was statistically insignificant (p> 0.05). These findings might be influenced by a small sample size of male animals (n=90) as compared to female animals (n=320). Findings by other researchers (Mellau et al 2009; Ferede et al 2011; Berhe et al 2007; Desefu et al 2011; Din et al 2013), reported higher Brucella prevalence in female animals as compared to male animals, although no controlled study has been conducted on the relative susceptibility of female and male cattle to brucellosis basing on the reactor rates. Less susceptibility of male animals to Brucella infections may be due to lack of erythritol in males (Ferede et al 2011). Moreover, Ferede et al (2011) revealed that in male animals Brucella infections limited to testes result into non reactors or reactors showing low antibody titers. Seroprevalence may increase with age as a result of prolonged exposure to pathogens particularly in traditional husbandry practices where females are maintained in herds for longer periods of time than males (Mergesa et al 2011). In the study areas females are maintained in herds for extended period of time thus having ample time for exposure to the pathogen and being source of infection for other animals.

With regard to the herd size, a slightly higher (23.1%) seroprevalence was observed in small herds as compared to large herds (21.3%). The difference, however, had no statistical significance. These findings are in agreement with the work done by Jergefa et al (2009) who recorded the average prevalences of 4.5% in small herds (≤ 16 animals) and 3% in large herds (> 16 animals) with no statistically significant difference. Contrary to our findings some other studies (Berhe et al 2007; Swai et al 2010; Al-Majali et al 2009) reported higher prevalences of 66.8%, 7.6% and 73%, respectively in large herds than prevalences of 28.6%, 2.2% and 15.0% in small herds, respectively. Larger herds provide more chances for contact between infected and non infected animals (Al-Majali et al 2009). The current observation might be influenced by the small sample size of small herds (n=13) tested as compared to large herds (n=47).

In the current study, there was no positive reactor among young animals while adults had a seroprevalence of 7.6%. This observed difference in seroprevalence between the two age categories was statistically significant. The association of adults with seropositivity to brucellosis is consistent with the findings of studies both in the country (Swai et al 2010) and elsewhere (Berhe et al 2007; Degefu et al 2011; Al-Majali et al 2009). Age is one of the intrinsic factors which influence the susceptibility to Brucella infection. Young and sexually immature animals are believed to be more resistant to primary infection and frequently clear infection although latent infections do occur (Degefu et al 2011). Growth and multiplication of Brucella organisms are stimulated by sex hormones and erythritol which tend to increase in concentration with age and sexual maturity (Ferede et al 2011). Swai et al (2010) on the other hand associated higher seroprevalence of brucellosis in adult animals with under nutrition, stress and lower immunity that develops following acute infection.

Risk factors influencing Brucella seropositivity

In this study, contact with small ruminants showed to have a significant effect on the serological prevalence of bovine brucellosis (p=0.03) in the study area. Similar observations have been previously reported by other researchers (Abbas et al 2002; Al-Majali et al 2009; Omer et al 2000; Swai et al 2010). During this study it was observed that, some livestock keepers practice multiple livestock herding particularly mixing cattle with goats and sheep. Studies have shown that, herds with multiple livestock species have high odds of seropositivity to Brucella, suggesting possibility of cross species transmission of Brucella (Mergesa et al 2011), and bearing in mind that in the current study area there was no history of vaccination against brucellosis as it was reported by District Livestock Officers in the study area. Multiple livestock species herding especially keeping of small ruminants along with cattle has been reported by many researchers as a risk factor for seropositivity to Brucella infection (Abbas et al 2002).

Another risk factor for bovine brucellosis in the study area was improper disposal of aborted materials (p=0.03). Only a small proportion (18.3%) of the interviewed participants practice proper disposal of aborted materials. Contamination of the environment with aborted materials, lochia, urine and uterine discharges have been documented to be major sources of infection to animals (Blood and Radostitis, 1990). Though Brucella is sensitive to direct sunlight, in dry conditions they survive if embedded in protein like aborted materials (Davies and Casey 1973). Leaving aborted materials to decay on grazing land as it was observed during this study may become a potential source of infection during grazing. Studies have indicated that Brucella can survive for 42 days (Baek et al 2003) to 75 days (King 1957) in aborted materials and/or uterine exudates. Blood and Radostitis (1990) indicated that, Brucella organisms can survive in the grass for varying periods of time with infectivity persisting for up to 100 days depending on the season. It has been also reported that under ambient temperature (120 C -200 C) and relative humidity (40%), Brucella organisms can survive in aborted fetuses in sheds and in liquid manure for up to 8 months (Bishop et al 1994), these conditions are important in this as in the study area almost the same conditions do prevail . Moreover animals get infection by contact with infected aborted materials (Mai et al 2012). Livestock keepers should either bury or burn aborted materials.

Herds in contact with dogs was another factor which significantly (p=0.01) affect the prevalence of bovine brucellosis in the study area. During this study, it was observed that livestock keepers use dogs as guardians during grazing. Forbes (1990) reported naturally acquired infection of dogs with B. abortus from infected cattle and demonstrated horizontal transfer of infection (dog to dog, cattle to dog, dog to cattle and dog to human) and that dogs with naturally acquired infections with B. abortus play important role in the epidemiology of bovine brucellosis. The relationship between infected dogs and outbreak of brucellosis in cattle has been demonstrated (Prior 1976; Forbes 1990). Dogs can also acquire Brucella infection through access to infected aborted materials from cattle (Baek et al 2003). Infected dogs can shed organisms into environment via urine/ faeces, vaginal secretions, aborted fetuses and hence cattle may get infected when grazing on contaminated pasture (George 1994; Zoha and Carmichael 1982). Brucella can survive for 30 days in urine and faeces (King 1957; Kerimov 1983). Moreover, it was observed during this study that livestock keepers feed aborted materials to dogs. Forbes (1990) indicated that, dogs carrying pieces of placenta or aborted fetuses from one place to another cause direct exposure to cattle.

Knowledge, attitudes and practices regarding brucellosis

Knowledge of a disease is a crucial step in the development of prevention and control measures (Tschopp et al 2011). Most of livestock keepers (90.0%) are not knowledgeable and aware of brucellosis and its zoonotic potential. Lack of knowledge and awareness about the disease and information on the zoonotic potential of brucellosis signify that farmers do not take required precautions when handling Brucella infected animals; and products and by products from infected animals thus jeopardizing their health. Moreover, with these results it is obvious that no precaution is taken to prevent spread of the disease to other herds within or outside the study area. The perception that brucellosis can be cured and the habit of people selling diseased animals either to the market or other livestock keepers as it was observed during this study can lead into propagation of the disease to other areas or herds which are not infected. Holt et al (2011) indicated that, selling infected animals at the market may increase transmission of brucellosis not only between households in the same village but also between villages and even larger geographical areas. In Tanzania, The Animal Disease Act, 2003 and its Regulation, 2007, give provisions for the disposal of Brucella reactor animals, however enforcement of such regulations to ensure compliance from farmers need to be put in place. Animals should be tested, reactors separated from the healthy animals and slaughtered. Livestock keepers in the study area showed very little awareness regarding isolation of Brucella infected animals and others even attempted to treat, both of these observations lead to propagation of the disease. Bruner et al (1966) pointed out that; animals are not usually given antimicrobials for prophylaxis or therapy against Brucella infection as they cause L-transformation on the cell wall thereby possibly creating carrier animals. In the study area, livestock keepers also do not separate animal (s) that abort. Holt et al (2011) indicated that failure to separate animals that abort is one of the major risk factors for disease transmission between animals as susceptible animals can be infected via contact with aborted materials or products of parturition.Uncontrolled movement of livestock is another practice which was noted in the study area. Haphazard animal movement can lead to dissemination of a disease to other places where disease is not present.

Conclusions

• The current study has revealed that bovine brucellosis was prevalent in Kibondo and Kakonko Districts.
  
  
• There was lack of knowledge and awareness about the disease and information on the zoonotic potential of brucellosis

Acknowledgements

SADC-TAD is acknowledged for financial support toward this study. Authors are also grateful to all the people who rendered assistance during data collection.

Conflict of interest

The authors declare that they have no conflict of interest.

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Received 16 February 2015; Accepted 14 April 2015; Published 3 June 2015

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