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Risk factors associated with contagious caprine pleuro-pneumonia in goats in pastoral areas in the Rift Valley region of Kenya
Preventive Veterinary Medicine 132 (2016) 107–112
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Risk factors associated with contagious caprine pleuro-pneumonia in goats in pastoral areas in the Rift Valley region of Kenya K.A. Kipronoh a,b,∗ , J.N. Ombui b , Y.S. Binepal d , H.O. Wesonga e , E.K. Gitonga e , E. Thuranira d , H.K. Kiara c a
Kenya Agricultural and Livestock Research Organization, Perkerra Research Centre, P.O. Box 32, Marigat, Kenya University of Nairobi, Faculty of Veterinary Medicine, Department of Public Health, Pharmacology and Toxicology, P.O. Box 29053, 00625 Kangemi. Nairobi Kenya c International Livestock Research Institute, P.O. Box 30197, Nairobi, Kenya d Kenya Agricultural and Livestock Research Organization, Biotechnology Research Centre, P.O. Box 57811, Nairobi, Kenya e Kenya Agricultural and Livestock Research Organization, Veterinary Research Institute, P.O. Box 32, Kikuyu, Kenya b
a r t i c l e
i n f o
Article history: Received 18 November 2015 Received in revised form 31 August 2016 Accepted 31 August 2016 Keywords: Contagious caprine pleuro-pneumonia Risk factors Pastoral areas Goats Kenya
a b s t r a c t A cross-sectional study to determine risk factors associated with sero-prevalence of contagious caprine pleuro-pneumonia (CCPP) in goats was carried out between the months of March, 2014 and March, 2015 in Pokot East, Turkana West and Kajiado Central Sub-counties. A semi-structured questionnaire focusing on risk factors for CCPP was completed for each flock whose serum samples were collected. A logistic regression model was developed to assess the association between the risk factors and CCPP seropositivity. Of the 54 flocks, 49 (90.7%) presented at least one sero-positive animal. Two hundred and four of the 432 goats tested sero-positive at monoclonal antibody based competitive Enzyme-linked immunosorbent assay (c-ELISA), hence a sero-prevalence of 47.2% (95% CI = 42.5– 51.9). Previous exposure of flocks to CCPP (p < 0.001, OR = 52.8; CI = 6.45, 432), distant sources of veterinary drugs (p < 0.001, OR = 6.17; CI = 3.41, 11.1), movement of goats to dry season feeding areas (p < 0.001, OR = 4.31; CI = 2.39, 7.75) and markets as a source of new introductions to the flock (p = 0.033, OR = 1.86; CI = 1.05, 3.27) were identified as risk factors significantly associated with CCPP sero-prevalence. The findings provide further evidence supporting the high prevalence and endemic state of the disease in pastoral flocks and hence there is need for adequate measures to be put in place to control the disease effectively. © 2016 Published by Elsevier B.V.
1. Introduction Contagious caprine pleuro-pneumonia (CCPP) is a highly contagious and often fatal disease of goats caused by Mycoplasma capricolum sub. spp. capripneumonia (mccp). CCPP is characterized by cough, severe respiratory distress, pyrexia (40.5–41.5 ◦ C), nasal discharge, which is catarrhal at the beginning and becomes muco-purulent in the later stage of disease. In chronic cases, the nasal discharges become thick and pasted on the nostrils. At this stage, animals show sporadic coughing, emaciation, and diarrhoea (Radostitis et al., 2006). Cases of CCPP result in variable but often high morbidity and mortality rates in susceptible flocks of all ages and in both sexes, and abortions in pregnant goats is common (OIE,
∗ Corresponding author at: Kenya Agricultural and Livestock Research Organization, Perkerra Research Centre, P.O Box 32, Marigat, Kenya. E-mail address: [email protected] (K.A. Kipronoh). http://dx.doi.org/10.1016/j.prevetmed.2016.08.011 0167-5877/© 2016 Published by Elsevier B.V.
2014). The disease is a major constraint to the goat industry in developing countries and is endemic in Africa, the Middle East and Asia (Manso-Silván et al., 2007; Nicholas and Churchward, 2012). Since the disease occurs in epidemics, antibiotic treatment, as the only control measure would be very un-economical. Vaccination associated with antibiotic treatment is the most effective strategy and antibiotics such as the tetracyclines, fluoroquinolones and the macrolide family are generally effective clinically if used early enough (Ozdemir et al., 2005). A precise description of the distribution of CCPP is not available mainly due to a lack of highly sensitive and specific diagnostic tests and difficulty of identification of the organism causing the disease (Nicholas, 2002). What is certain is that the disease is present in Africa and the Middle East where it has been reported in 30 countries in these continents (Thiaucourt and Bolske, 1996) and represents a significant threat to many disease-free areas as demonstrated by isolation (the confirmatory test required by the OIE) and molecular characterization of Mccp isolates (Woubit et al.,
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2004). The disease is included in the list of notifiable diseases by World Organization of Animal Health (OIE) because of its very high morbidity and mortality rates causing significant socio-economic impact once introduced into a country. A specific risk for the disease is that it has been spreading beyond its traditional distribution area with effects on livelihoods and international trade (AU-IBAR, 2015). According to Pan African Animal Health Yearbook, seven countries reported the occurrence of CCPP in 2011, with Ethiopia, Somalia and Tanzania consistently reporting the disease since 2008 to then (AU-IBAR, 2014). The disease seems to be confined to the eastern and central Africa regions based on the reports received. CCPP is transmitted by direct contact through inhalation of infective aerosols from infected goats by susceptible goats. The disease is highly contagious and only brief periods of contact are necessary for successful transmission (Thiaucourt and Bolske, 1996). Disease outbreaks often occur after heavy rains and after cold spells probably because recovered carrier animals start shedding the mycoplasmas after the stress of sudden climatic change. It is these latent carriers that have been reported responsible for the perpetuation of the disease in a flock (Thiaucourt and Bolske, 1996; Wesonga et al., 1998). Several studies on CCPP outbreak investigations and isolation of the causative agent have been conducted. However, information on sero-prevalence and associated risk factors is scanty. The current study was conducted in Turkana, Baringo and Kajiado Counties of Rift valley region of Kenya to estimate the risk factors associated with prevalence of the disease in pastoral areas and provide information useful for making informed decisions in developing and recommending targeted control measures for effective control. 2. Materials and methods 2.1. Selection of study sites The sites were purposely selected to represent different epidemiologic states of the disease; border counties where there is high animal contact across the borders which is a risk factor and a county which does not share international boundary. The study areas were stratified into livestock grazing regions based on the direction of livestock movement (migratory routes) to the three neighbouring countries that include Oldonyo-Orok group ranch and Torosei in Kajiado Central Sub-county with migratory routes between Kenya and Tanzania; Oropoi and Loremet grazing areas in Turkana West Sub-county with migratory routes between Kenya and Uganda as well as South Sudan. These grazing areas were selected to represent sites that share international boundaries where animals occasionally mix with those in adjoining areas of the neighbouring countries in dry season grazing, watering points and markets. Silale and Orus grazing areas in Pokot East Sub-county were selected to represent areas far from international boundaries. 2.2. Study design and sampling A cross-sectional study was carried out between March 2014 and March 2015 using multistage random sampling method. A list of all locations and their sub-locations were obtained through the assistance of the local administration. From the list, one location per ward and one sub-location in each location were randomly selected using random number tables. A list of all adakaars/villages were obtained in each sub location selected. Three villages and three livestock owners from each of the villages whose flocks had no history of vaccination for at least a year prior to the commencement of the survey were randomly selected to participate in the completion of the structured questionnaires. Finally, systematic random
sampling was applied to select goats from each flock to be bled for serum sample collection. A total of 18 Adakaars/villages were used for the study. 2.3. Questionnaire data collection A pre-tested semi-structured questionnaire focusing on risk factors for contagious caprine pleuropneumonia was administered to the participating pastoralists in an interactive manner through personal interviews to obtain in-depth information on pastoralists’ knowledge, attitudes and practices that could be potential risks factors associated with outbreaks of the disease. Piloting of the questionnaire was conducted in sites where the study was to be done and three pastoralists from each of the study areas were requested to respond to the questionnaire. The aim was to assess the timing of interview, the respondents’ reactions to the question format, wordings and order of asking questions and ensure that the final questionnaire to be used was understandable. The results of the questionnaires were reviewed and revisions were made accordingly considering the significant problems detected during pre-testing. The questionnaire was designed to record the respondents’ location, household characteristics and livestock management practices. A number of open-ended questions were included in the questionnaire to allow the pastoralists an opportunity to provide their perspectives and experiences on treatments and methods available for CCPP control. 2.4. Collection of blood samples and serology The number of goats bled for serology were determined using the formula for sample size estimation; n = Z2 ␣pq/L2 , (Martin et al., 1987). Where, n = sample size, Z␣ = normal deviate (1.96) at 5% level of significance, p = estimated prevalence, q = 1-p and L = precision of estimate usually at 5%. A priori prevalence of 30% was used based on the findings by Wafula, (2006) in a study done in Turkana. From the formula, the sample size was calculated as follows; n = 1.962 × 0.3(1 − 0.3)/0.052 n = 3.8416 × 0.21/.0025 = 322.72–323. To adjust for potential non-compliance and design effect, the calculated sample size was increased by 30% bringing the totals to 419.9 ∼ 420. Further, from the calculated sample size, 7.78 goats were to be selected for biological sample collection from each pastoralist which was rounded off to 8 hence the final sample size was put at 432 goats to be selected from 54 flocks. Blood samples were collected from the jugular vein in clean sterile vacutainers and allowed to clot. Sera were separated and kept frozen at −20 ◦ C until used for serology. Monoclonal antibody based competitive Enzyme-linked immuno-sorbent assay (c-ELISA) was used to assess presence of specific antibodies against Mycoplasma capricolum sub. spp. capripneumonia (mccp) using the procedure described by Peyraud et al., 2014. The test kit was supplied by CIRAD-EMVT, France. The test has been evaluated and it has a strict specificity of 99.9%. It allows the detection of positive sera in CCPP-infected herds, but its sensitivity at the individual level has not yet been fully evaluated and thus true prevalence of the disease cannot be computed (OIE, 2014). The test sera were examined in 96-well flat bottom microplates coated with Mycoplasma F38 antigen diluted with 0.01 mol/L phosphate-buffered saline, pH 7.2–7.4. There were control sera of strong positive serum, weak positive serum, a test laboratory positive serum and monoclonal antibody (Mab) per plate. The plate was incubated at 37 ◦ C for 1 h, washed with
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Table 1 Demographic and social characteristics of the communities that participated in selected Counties of Rift Valley region of Kenya. County Characteristic
Category
Baringo (n = 18)
Kajiado (n = 18)
Turkana (n = 18)
Gender of pastoralist
Male Female 18–35 36–45 46–55 56–65 66–75 None Primary Secondary Tertiary Sedentary Nomadic Transhumance Crops Livestock Small scale business Employment Others Cattle Sheep Goats Camel Donkey Poultry Number of goats per household Private paddocks Communal fields Self Veterinary personnel Agro-vet. shop attendant
17 (94.4) 1(5.6) 3 (16.7) 7 (38.9) 5 (27.8) 2 (11.1) 1 (5.6) 14 (77.8) 4 (22.2 0 (0.0) 0 (0.0) 0 (0.0) 9 (50) 9 (50) 2.75 90.03 3.25 0.02 3.95 2 (11.1) 0 (0.0) 16 (88.9) 0 (0.0) 0 (0.0) 0 (0.0) 103 0 (0.0) 18 (100.0) 18 (100.0) 0 (0.0) 0 (0.0)
18 (100.0) 0 (0.0) 7 (38.9) 4 (22.2) 2 (11.1) 3 (16.7) 2 (11.1) 13 (72.2) 3 (16.7) 1 (5.6) 1 (5.6) 0 (0.0) 2 (11.1) 16 (88.9) 0.00 94.92 4.73 0.35 0.00 11 (61.1 2 (11.1) 5 (27.8) 0 (0.0) 0 (0.0) 0 (0.0) 90 0 (0.0) 18 (100.0) 18 (100.0) 0 (0.0) 0 (0.0)
18 (100.0) 0 (0.0) 17 (94.4) 1 (5.6) 0 (0.0) 0 (0.0) 0 (0.0) 17 (94.4) 1(5.6) 0 (0.0) 0 (0.0) 0 (0.0) 18 (100.0) 0 (0.0) 0.00 100.00 0.00 0.00 0.00 0 (0.0) 0 (0.0) 18 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 65 0 (0.0) 18(100.0) 18 (100.0) 0 (0.0) 0 (0.0)
Age of pastoralist
Pastoralist education level
Way of living
Proportion of household income
Livestock enterprise
Average flock size Feeding/browse area Treatment of sick goats
phosphate-buffered saline (PBS) and developed for optical density (OD) reading at 405 nm in an ELISA reader. Optical density values of over 50% were considered positive.
Lemeshow goodness of fit test and the Cox and Snell and Nagelkerke R square values which provided indication of the amount of variation in the independent variable explained by the fitted model.
2.5. Data analysis
3. Results
Questionnaire and serology data were entered in Microsoft Excel spreadsheet. Statistical analyses were carried out using the IBM SPSS statistics 20 software. Odds ratios (OR) and 95% confidence levels (CIs) were calculated to measure the association of the potential risk factors and prevalence of CCPP using binary logistic regression. Univariate models were first run to assess the association between CCPP sero-prevalence and potential risk factors. The risk factors assessed were sex, age, county, location, flock size, source of introductions to the flock, water source, grazing area, season, access to veterinary drugs/services, vaccination status and previous exposure of goats to CCPP. The significance level was set at p < 0.10 based on the likelihood ratio test. A multivariate logistic regression model was subsequently built using significant variables in the univariate analysis. Model building used a stepwise forward method (Hosmer and Lemeshow, 1989) to decide on the factors and significant interactions to include in the model using the likelihood ratio test (P < 0.05). All the significant risk factors were initially included in the model. The strength of association between the risk factor and CCPP sero-positivity was estimated using the odds ratios (OR) which were directly derived from the coefficient estimates from the logistic regression models. Odds ratio is ‘the increase (or decrease if the ratio is less than 1) in odds of being in one outcome category when the value of the predictor increases by one unit’. For each of OR, there is a 95% CI displayed giving a lower and upper value and encompasses the true value of OR and gives confidence that we have in it being an accurate representation of the true value from the population. Model fit was examined using the Hosmer and
A total of 54 flocks from different owners were involved in the study. A summary of the demographic and social structure of the communities that were selected to participate in the study is shown in Table 1. Nomadism and transhumance were the only ways of keeping livestock reported from this study which are typical for pastoral communities. Almost all the respondent pastoralists (98.1%) were males in the age category of 18–35 years, the majority of whom (81.5%) had no formal education and livestock was their main source of livelihood. Rearing of goats was the priority enterprise for the nearly (72.2%) all of the households followed by cattle and sheep in that order. The average herd size per household was 86 goats. Forty nine of the 54 flocks presented at least one seropositive animal giving an overall flock sero-prevalence of 90.7%. Two hundred and four of the 432 goats tested positive by monoclonal antibody based competitive Enzyme-linked immunosorbent assay (c-ELISA) test, hence a sero-prevalence of 47.2% (95% CI = 42.5–51.9). The results of univariate analysis indicated that a number of factors associated with CCPP sero-prevalence. Among the variables, locations, market as source of goats introduced to the flock, sources of water for goats, access to veterinary drugs at distant markets, history of recent vaccination of flocks and previous exposure to CCPP were selected (p < 0.10) for multivariate analysis. Age and sex of the goats were not significantly associated with CCPP sero-prevalence with statistical levels of p = 0.231 and p = 0.107 respectively. Other factors that were not significantly associated with sero-prevalence of the disease were size of the flocks and season of the year (Table 2).
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Table 2 Univariate analysis of factors associated with CCPP sero-prevalence. Variable
Sex Age
County
Location
Flock size
Source of new introductions Source of water
Keeping goats in dry season feeding area Season of the year
Distant access to veterinary drugs Vaccination Previous exposure to CCPP
Category
Male Female weaners Yearling Adults Baringo Turkana Kajiado Kalobeyei Lokichoggio Naudo Oldonyo Orok Orus Torosei 1–100 101–200 201–300 Market Gifts (dowry) River Stream Borehole Dam Shallow well Yes No Wet season Dry season Throughout Distant market Local market Yes No Yes No
No. of goats testing positive
Prevalence (%)
72 132 39 34 131 42 92 70 43 49 16 46 26 24 162 34 8 65 24 17 32 65 26 64 64 140 151 41 11 151 53 32 172 203 1
53.3 44.4 42.4 42.0 50.6 29.2 63.9 48.6 59.7 68.1 22.2 63.9 36.1 33.3 49.4 38.6 50.0 0.58 0.3 21.3 50.0 67.7 36.1 53.3 57.1 43.8 49.8 45.8 41.7 62.9 27.6 66.7 44.8 48.8 6.2
95% C.I.
P-value
Lower
Upper
44.9 38.8 32.2 31.1 44.5 21.7 56.0 40.4 48.8 57.1 11.3 53.0 25.2 22.4 44.0 28.2 25.5 0.5 0.2 10.8 38.3 58.2 25.1 44.8 47.9 38.3 44.3 34.2 21.6 57.0 21.0 52.6 39.8 44.0 1.8
61.8 50.1 52.6 52.9 56.7 36.6 71.7 56.8 70.6 79.0 33.1 74.8 47.0 44.3 54.8 49.1 74.5 0.7 0.4 31.7 61.7 77.3 47.1 61.9 66.4 49.2 55.4 57.4 61.8 68.9 34.2 80.7 49.8 53.6 30.5
0.107 0.231
<0.001
<0.001
0.196
<0.001 <0.001
0.014 0.646
<0.001 0.004 0.001
Table 3 Multivariate analysis of risk factors associated with CCPP sero-prevalence. Variable

S.E.
Wald
EXP()
95% C.I. for EXP()
p-value
Previous exposure to CCPP 1 = Yes, 0 = No Access of veterinary drugs at distant markets 1 = Distant agro-veterinary shops, 0 = Local market Moving goats to dry season feeding areas 1 = Yes, 0 = No Markets as a source of new introductions into the flock 1 = Market, 0 = Gifts (dowry)
3.966 1.819
1.1 0.3
13.7 36.4
52.8 6.17
6.45 3.41
432 11.1
<0.001 <0.001
1.46
0.3
23.7
4.30
2.39
7.75
<0.001
0.618
0.3
4.6
1.86
1.05
3.27
0.033
N = 432, −2Log-likelihood = 332.062 df 6; p = 0.392.
The final multivariate logistic regression model for CCPP seroprevalence is shown in Table 3. The variables considered as risk factors in the model were; previous exposure of flock to CCPP (p < 0.001, OR = 52.8; CI = 6.45, 432), access of veterinary drugs at distant markets (p < 0.001, OR = 6.17 CI = 3.41, 11.1), movement goats to dry season feeding areas (p < 0.001, OR = 4.31 CI = 2.39, 7.75) and markets as a source of new introductions to the flock (p = 0.033, OR = 1.86 CI = 1.05, 3.27). The final model fitted well (Hosmer and Lemeshow, 1989; 2 = 6.289, p = 0.392). Between 25.1 and 33.8% variability was explained by the set of variables as indicated by Cox and Snell and Nagelkerke R square values. There were no significant interactions in the model. 4. Discussion The general characteristics of the study population were typical of an extensive pastoral production system where nomadism and transhumance were practiced by 53.7% and 46.3% of the pastoral-
ists respectively. These traditional livestock production systems are common in most African countries and enhances the spread of CCPP as animals congregate during grazing and watering (Lefevre et al., 1987) given that the disease is highly contagious and infectious and is transmitted by direct contact through inhalation of infective aerosols from infected goats by susceptible goats. In the current study, almost all the flocks (90.7%) presented at least one CCPP sero-positive animal which together with the high regional animal sero-prevalence of 47.2% (95% CI = 42.5–51.9), confirm the endemic state of the disease in the region. The findings were consistent with the results obtained by Peyraud et al., 2014 in a similar study that reported between flock CCPP sero-prevalence varying from 6 to 90% in Narok County although the findings from our study were more specific in reference to the timing of our study and the selection of the study areas. There was a variation in CCPP sero-prevalence in the different counties and locations selected in the study. A significantly higher sero-prevalence of 63.9% (95% CI = 56.0–71.7) and 48.6
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(95% CI = 40.4–56.8) was recorded in study areas in Turkana West Sub-county which shares boundaries with South-Sudan to the North-West and Uganda to the West and Kajiado Central Sub county which shares boundary with Tanzania to the West respectively while study areas in Pokot East Sub-counties which are far from international boundaries had a prevalence of 29.2% (95% CI = 21.7–36.6). A similar observation was reported by Wafula (2007) in a study done in the same region using complement fixation test. The results are a pointer to the high risk due to the porous nature of the international borders of the country and hence there is need for cross-border harmonization of disease control programs including routine vaccination among the neighbouring pastoral communities for effective management of CCPP outbreaks and spread. In this study, none of the animal level variables; sex and age of goats were significantly associated with CCPP sero-positivity in this study. The observation agrees with the reports by Mekuria and Asmare (2010), Eshetu et al. (2007) and OIE (2014) which concluded the above factors to have no role in CCPP epidemiology. However, the results were contradictory to the findings by Mohammed (2008) and Regassa et al. (2010) that reported significant sex difference in CCPP sero-prevalence and a study by Matios et al. (2014) which reported a significantly higher prevalence in the old age category. This may be due to older animals having been at risk of exposure for a longer period than young animals and not necessarily as a result of recent infection. The association of history of exposure of flock to CCPP was expected. Infected goats remain carriers even when treated with the available antibiotics and are a potential risk to the healthy goats in the flock and those they come in contact at feeding areas, watering points and markets. Goats that were purchased from markets were about 2 times more likely to be sero-positive to the disease than the ones offered to households as gifts and dowry. Normally, goats with chronic illness some of which might be infected with CCPP are candidates for culling and most of them are sold in local markets. The disease is commonly spread by direct contact (aerogenic route, through droplets released during coughing) and a very short period of intimate contact is sufficient to transmit the disease (Thiaucourt and Bolske, 1996). A single surviving seropositive goat from a natural outbreak in Thrace region of Turkey for example, was able to infect all 10 disease-free contacts within 2 weeks when kept in close confinement (Ozdemir et al., 2005). Coincidentally, results from the current study showed a strong association between serological prevalence and movement of goats to dry season feeding areas. The recurrent drought episodes commonly experienced in most pastoral regions of the country is a reason for movement of flocks to dry season feeding areas in search of adequate browse and water for goats resulting in a high rate of contact of flocks. The phenomenon has been reported to be ideal for the transmission of CCPP (Seifert, 1996). Cross-border movements were commonly reported in study areas in Turkana West and Kajiado Central which were very remote and as such, the pastoralists had never been visited by veterinary extension officers who are expected to implement the disease control policy. Difficulty in accessing veterinary health services remain a challenge to improving productivity of livestock enterprises pastoral areas. In this study, there was a risk of CCPP sero-prevalence with access to drugs from distant markets. Goats from flocks whose owners could not easily access veterinary drug outlets were 6 times more likely to be sero-positive than those within a close range of distances (less than 20 kilometers) from the veterinary service providers. Most villages in the study areas were beyond this radius (up to 100 Kilometers away) in hilly terrains and transport was unavailable. Moreover, there were frequent reports of insecurity in some areas that were consequently shunned by veterinary ser-
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vice providers (Kipronoh et al., 2016). As a result, treatment of sick animals were delayed and chances of recovery was low. Majority of the pastoralists made their own diagnoses of diseased goats and administered drug combinations that they thought were appropriate. In some areas of Baringo County for example, the pastoralists relied on traditional herbal concoctions whose efficacy against CCPP is unknown. In most cases, sick goats were not promptly or properly treated which could be reason for development of carrier states that plays an important role in the transmission of the disease. The findings are in agreement with a previous report by Sori (1999) which indicated that the impact of insufficient veterinary services in mobile livestock production systems increases the spread of diseases. 5. Conclusion The study provided information on risk factors associated with occurrence of CCPP in goats and further evidence to support the high prevalence and endemic state of the disease in Kenya. The findings suggest that the pastoral flocks are at risk of infection with CCPP due to previous exposure of flocks to CCPP, difficulty in accessing veterinary drugs, movement of goats to dry season feeding areas and introduction of goats into flocks from markets. The above risk factors were found to be significantly associated with CCPP sero-positivity. Consequently there is a need for adequate and coordinated measures to be put in place to control the disease effectively for improved productivity of the goat enterprise in the country. Acknowledgement The study was jointly supported through funding from the Kenya Agricultural and Livestock Research Organization (KALRO) through KAPAP PhD Scholarship grant-KARI/3/047/48 and Kenya’s National Commission of Science, Technology and Innovation (NACOSTI) through NACOSTI/RCD/5TH CALL PhD/001 grant. The authors gratefully acknowledge all the pastoralists and village/adakaar leaders who participated in the study for their maximum cooperation in getting samples for serology. We also appreciate the effort made by the Sub county veterinary officers and their field staff in facilitating the administration of questionnaires and sample collection. References AU-IBAR, 2014. Pan African Animal Health Yearbook 2014. Pan African Animal Health Yearbook, 2014 (accessed 04.03.2016) http://www.au-ibar.org/panafrican-animal-resources-yearbook. AU-IBAR, 2015. Standard Methods and Procedures (SMPs) for Contagious Caprine Pleuropneumonia (CCPP) in the Greater Horn of Africa, Nairobi (accessed 04.03.2016) http://www.au-ibar.org/component/jdownloads/viewdownload/ 76-tmt/2417-tmt-20151218-smp-ccpp-en. Eshetu, L., Yigezu, L., Asfaw, Y., 2007. A study on contagious caprine pleuropneumonia (CCPP) in goats at an export oriented abattoir Debrezeit, Ethiopia. Trop. Anim. Health Prod. 39, 427–432. Hosmer, D.W., Lemeshow, S., 1989. Applied Logistic Regression. Wiley, NewYork. Kipronoh, K.A., Kiara, H.K., Binepal, Y.S., Thuranira, E., Ombui, J.N., 2016. Pastoralists’ perception of constraints affecting goat production in the Rift Valley region of Kenya. Livestock Research for Rural Development. 28, Article #33. http://www.lrrd.org/lrrd28/3/kipr28033.html (accessed 02.03.2016). Lefevre, P.C., Jone, G.E., Ojo, M.O., 1987. Pulmonary mycoplasmosis of small ruminants revue scientifique et technique. Office Int. des ëpizooties 6 (3), 759–799. Manso-Silván, L., Perrier, X., Thiaucourt, F., 2007. Phylogeny of the Mycoplasma mycoides cluster based on analysis of five conserved protein-coding sequences and possible implications for the taxonomy of the group. Int. J. Syst. Evol. Microbiol. 57 (Pt. 10), 2247–2258, 10. Martin, S.W., Meek, A.H., Willeberg, P., 1987. Veterinary Epidemiology Principles and Methods. Iowa State University Press, Ames Iowa (343 pp.). Matios, L., Tesfaye, S., Gelagay, A., Eyop, E., Gebremikael, D., Tadele, T., 2014. Seroprevelence of contagious caprine pleuropneumonia and field performance
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of inactivated vaccine in Borana pastoral area, Southern Ethiopia. Afr. J. Microbiol. Res. 8 (June (24)), 2344–2351. Mekuria, S., Asmare, A., 2010. Cross-sectional study on Contagious Caprine Pleuro Pneumonia in selected woredas of sedentary and pastoral production systems in Southern Ethiopia. Trop. Anim. Health Prod. 42, 65–72. Mohammed, H., 2008. Sero-epidemiological Study Contagious Caprine Pleuropneumonia in Eastern Ethiopia Dvm Thesis. Faculty of Veterinary Medicine, Haramaya University, Ethiopia. Nicholas, R., Churchward, C., 2012. Contagious caprine pleuropneumonia: a new aspencts of an old disease. Transbound. Emerg. Dis. 59, 189–196. Nicholas, R.A.J., 2002. Contagious caprine pleuropneumonia. In: Tempesta, M. (Ed.), Recent Advances in Goat Diseases. International Veterinary Information Service (IVIS), Ithaca Ny, pp. 1–6, A0907–0802 www.ivis.org. OIE, 2014. Manual of diagnostic tests and vaccines for terrestrial animals. CCPP (Chapter 2.4.6). Ozdemir, U., Ozdemir, S., March, J.B., Churchwood, C., Nicholas, R.A.J., 2005. Outbreaks of CCPP in the Thrace region of Turkey. Vet. Rec. 156, 286–287. Peyraud, A., Poumarat, F., Tardy, F., Manso-Silván, L., Hamroev, K., Tilloev, T., Amirbekov, M., Tounkara, K., Bodjo, C., Wesonga, H., Nkando, I., Jenberie, S., Yami, M., Cardinale, E., Meenowa, D., Jaumally, M.R., Yaqub1, T., Shabbir, M.Z., Mukhtar, N., Halimi, M., Ziay, G.M., Schauwers, W., Noori, H., Rajabi, A.M., Ostrowski, S., Thiaucourt, F., 2014. An international collaborative study to determine the prevalence of contagious caprine pleuropneumonia by monoclonal antibody-based cELISA. BMC Vet. Res. 2014 (10), 48, http://dx.doi. org/10.1186/1746-6148-10-48. Radostitis, O.M., Gay, C.C., Hinchliff, W.K., Constable, D.P., 2006. Veterinary Medicine. A Text Book of the Disease of Cattle, Sheep, Pigs, Goats and Horses,
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Risk factors associated with contagious caprine pleuro-pneumonia in goats in pastoral areas in the Rift Valley region of Kenya K.A. Kipronoh a,b,∗ , J.N. Ombui b , Y.S. Binepal d , H.O. Wesonga e , E.K. Gitonga e , E. Thuranira d , H.K. Kiara c a
Kenya Agricultural and Livestock Research Organization, Perkerra Research Centre, P.O. Box 32, Marigat, Kenya University of Nairobi, Faculty of Veterinary Medicine, Department of Public Health, Pharmacology and Toxicology, P.O. Box 29053, 00625 Kangemi. Nairobi Kenya c International Livestock Research Institute, P.O. Box 30197, Nairobi, Kenya d Kenya Agricultural and Livestock Research Organization, Biotechnology Research Centre, P.O. Box 57811, Nairobi, Kenya e Kenya Agricultural and Livestock Research Organization, Veterinary Research Institute, P.O. Box 32, Kikuyu, Kenya b
a r t i c l e
i n f o
Article history: Received 18 November 2015 Received in revised form 31 August 2016 Accepted 31 August 2016 Keywords: Contagious caprine pleuro-pneumonia Risk factors Pastoral areas Goats Kenya
a b s t r a c t A cross-sectional study to determine risk factors associated with sero-prevalence of contagious caprine pleuro-pneumonia (CCPP) in goats was carried out between the months of March, 2014 and March, 2015 in Pokot East, Turkana West and Kajiado Central Sub-counties. A semi-structured questionnaire focusing on risk factors for CCPP was completed for each flock whose serum samples were collected. A logistic regression model was developed to assess the association between the risk factors and CCPP seropositivity. Of the 54 flocks, 49 (90.7%) presented at least one sero-positive animal. Two hundred and four of the 432 goats tested sero-positive at monoclonal antibody based competitive Enzyme-linked immunosorbent assay (c-ELISA), hence a sero-prevalence of 47.2% (95% CI = 42.5– 51.9). Previous exposure of flocks to CCPP (p < 0.001, OR = 52.8; CI = 6.45, 432), distant sources of veterinary drugs (p < 0.001, OR = 6.17; CI = 3.41, 11.1), movement of goats to dry season feeding areas (p < 0.001, OR = 4.31; CI = 2.39, 7.75) and markets as a source of new introductions to the flock (p = 0.033, OR = 1.86; CI = 1.05, 3.27) were identified as risk factors significantly associated with CCPP sero-prevalence. The findings provide further evidence supporting the high prevalence and endemic state of the disease in pastoral flocks and hence there is need for adequate measures to be put in place to control the disease effectively. © 2016 Published by Elsevier B.V.
1. Introduction Contagious caprine pleuro-pneumonia (CCPP) is a highly contagious and often fatal disease of goats caused by Mycoplasma capricolum sub. spp. capripneumonia (mccp). CCPP is characterized by cough, severe respiratory distress, pyrexia (40.5–41.5 ◦ C), nasal discharge, which is catarrhal at the beginning and becomes muco-purulent in the later stage of disease. In chronic cases, the nasal discharges become thick and pasted on the nostrils. At this stage, animals show sporadic coughing, emaciation, and diarrhoea (Radostitis et al., 2006). Cases of CCPP result in variable but often high morbidity and mortality rates in susceptible flocks of all ages and in both sexes, and abortions in pregnant goats is common (OIE,
∗ Corresponding author at: Kenya Agricultural and Livestock Research Organization, Perkerra Research Centre, P.O Box 32, Marigat, Kenya. E-mail address: [email protected] (K.A. Kipronoh). http://dx.doi.org/10.1016/j.prevetmed.2016.08.011 0167-5877/© 2016 Published by Elsevier B.V.
2014). The disease is a major constraint to the goat industry in developing countries and is endemic in Africa, the Middle East and Asia (Manso-Silván et al., 2007; Nicholas and Churchward, 2012). Since the disease occurs in epidemics, antibiotic treatment, as the only control measure would be very un-economical. Vaccination associated with antibiotic treatment is the most effective strategy and antibiotics such as the tetracyclines, fluoroquinolones and the macrolide family are generally effective clinically if used early enough (Ozdemir et al., 2005). A precise description of the distribution of CCPP is not available mainly due to a lack of highly sensitive and specific diagnostic tests and difficulty of identification of the organism causing the disease (Nicholas, 2002). What is certain is that the disease is present in Africa and the Middle East where it has been reported in 30 countries in these continents (Thiaucourt and Bolske, 1996) and represents a significant threat to many disease-free areas as demonstrated by isolation (the confirmatory test required by the OIE) and molecular characterization of Mccp isolates (Woubit et al.,
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2004). The disease is included in the list of notifiable diseases by World Organization of Animal Health (OIE) because of its very high morbidity and mortality rates causing significant socio-economic impact once introduced into a country. A specific risk for the disease is that it has been spreading beyond its traditional distribution area with effects on livelihoods and international trade (AU-IBAR, 2015). According to Pan African Animal Health Yearbook, seven countries reported the occurrence of CCPP in 2011, with Ethiopia, Somalia and Tanzania consistently reporting the disease since 2008 to then (AU-IBAR, 2014). The disease seems to be confined to the eastern and central Africa regions based on the reports received. CCPP is transmitted by direct contact through inhalation of infective aerosols from infected goats by susceptible goats. The disease is highly contagious and only brief periods of contact are necessary for successful transmission (Thiaucourt and Bolske, 1996). Disease outbreaks often occur after heavy rains and after cold spells probably because recovered carrier animals start shedding the mycoplasmas after the stress of sudden climatic change. It is these latent carriers that have been reported responsible for the perpetuation of the disease in a flock (Thiaucourt and Bolske, 1996; Wesonga et al., 1998). Several studies on CCPP outbreak investigations and isolation of the causative agent have been conducted. However, information on sero-prevalence and associated risk factors is scanty. The current study was conducted in Turkana, Baringo and Kajiado Counties of Rift valley region of Kenya to estimate the risk factors associated with prevalence of the disease in pastoral areas and provide information useful for making informed decisions in developing and recommending targeted control measures for effective control. 2. Materials and methods 2.1. Selection of study sites The sites were purposely selected to represent different epidemiologic states of the disease; border counties where there is high animal contact across the borders which is a risk factor and a county which does not share international boundary. The study areas were stratified into livestock grazing regions based on the direction of livestock movement (migratory routes) to the three neighbouring countries that include Oldonyo-Orok group ranch and Torosei in Kajiado Central Sub-county with migratory routes between Kenya and Tanzania; Oropoi and Loremet grazing areas in Turkana West Sub-county with migratory routes between Kenya and Uganda as well as South Sudan. These grazing areas were selected to represent sites that share international boundaries where animals occasionally mix with those in adjoining areas of the neighbouring countries in dry season grazing, watering points and markets. Silale and Orus grazing areas in Pokot East Sub-county were selected to represent areas far from international boundaries. 2.2. Study design and sampling A cross-sectional study was carried out between March 2014 and March 2015 using multistage random sampling method. A list of all locations and their sub-locations were obtained through the assistance of the local administration. From the list, one location per ward and one sub-location in each location were randomly selected using random number tables. A list of all adakaars/villages were obtained in each sub location selected. Three villages and three livestock owners from each of the villages whose flocks had no history of vaccination for at least a year prior to the commencement of the survey were randomly selected to participate in the completion of the structured questionnaires. Finally, systematic random
sampling was applied to select goats from each flock to be bled for serum sample collection. A total of 18 Adakaars/villages were used for the study. 2.3. Questionnaire data collection A pre-tested semi-structured questionnaire focusing on risk factors for contagious caprine pleuropneumonia was administered to the participating pastoralists in an interactive manner through personal interviews to obtain in-depth information on pastoralists’ knowledge, attitudes and practices that could be potential risks factors associated with outbreaks of the disease. Piloting of the questionnaire was conducted in sites where the study was to be done and three pastoralists from each of the study areas were requested to respond to the questionnaire. The aim was to assess the timing of interview, the respondents’ reactions to the question format, wordings and order of asking questions and ensure that the final questionnaire to be used was understandable. The results of the questionnaires were reviewed and revisions were made accordingly considering the significant problems detected during pre-testing. The questionnaire was designed to record the respondents’ location, household characteristics and livestock management practices. A number of open-ended questions were included in the questionnaire to allow the pastoralists an opportunity to provide their perspectives and experiences on treatments and methods available for CCPP control. 2.4. Collection of blood samples and serology The number of goats bled for serology were determined using the formula for sample size estimation; n = Z2 ␣pq/L2 , (Martin et al., 1987). Where, n = sample size, Z␣ = normal deviate (1.96) at 5% level of significance, p = estimated prevalence, q = 1-p and L = precision of estimate usually at 5%. A priori prevalence of 30% was used based on the findings by Wafula, (2006) in a study done in Turkana. From the formula, the sample size was calculated as follows; n = 1.962 × 0.3(1 − 0.3)/0.052 n = 3.8416 × 0.21/.0025 = 322.72–323. To adjust for potential non-compliance and design effect, the calculated sample size was increased by 30% bringing the totals to 419.9 ∼ 420. Further, from the calculated sample size, 7.78 goats were to be selected for biological sample collection from each pastoralist which was rounded off to 8 hence the final sample size was put at 432 goats to be selected from 54 flocks. Blood samples were collected from the jugular vein in clean sterile vacutainers and allowed to clot. Sera were separated and kept frozen at −20 ◦ C until used for serology. Monoclonal antibody based competitive Enzyme-linked immuno-sorbent assay (c-ELISA) was used to assess presence of specific antibodies against Mycoplasma capricolum sub. spp. capripneumonia (mccp) using the procedure described by Peyraud et al., 2014. The test kit was supplied by CIRAD-EMVT, France. The test has been evaluated and it has a strict specificity of 99.9%. It allows the detection of positive sera in CCPP-infected herds, but its sensitivity at the individual level has not yet been fully evaluated and thus true prevalence of the disease cannot be computed (OIE, 2014). The test sera were examined in 96-well flat bottom microplates coated with Mycoplasma F38 antigen diluted with 0.01 mol/L phosphate-buffered saline, pH 7.2–7.4. There were control sera of strong positive serum, weak positive serum, a test laboratory positive serum and monoclonal antibody (Mab) per plate. The plate was incubated at 37 ◦ C for 1 h, washed with
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Table 1 Demographic and social characteristics of the communities that participated in selected Counties of Rift Valley region of Kenya. County Characteristic
Category
Baringo (n = 18)
Kajiado (n = 18)
Turkana (n = 18)
Gender of pastoralist
Male Female 18–35 36–45 46–55 56–65 66–75 None Primary Secondary Tertiary Sedentary Nomadic Transhumance Crops Livestock Small scale business Employment Others Cattle Sheep Goats Camel Donkey Poultry Number of goats per household Private paddocks Communal fields Self Veterinary personnel Agro-vet. shop attendant
17 (94.4) 1(5.6) 3 (16.7) 7 (38.9) 5 (27.8) 2 (11.1) 1 (5.6) 14 (77.8) 4 (22.2 0 (0.0) 0 (0.0) 0 (0.0) 9 (50) 9 (50) 2.75 90.03 3.25 0.02 3.95 2 (11.1) 0 (0.0) 16 (88.9) 0 (0.0) 0 (0.0) 0 (0.0) 103 0 (0.0) 18 (100.0) 18 (100.0) 0 (0.0) 0 (0.0)
18 (100.0) 0 (0.0) 7 (38.9) 4 (22.2) 2 (11.1) 3 (16.7) 2 (11.1) 13 (72.2) 3 (16.7) 1 (5.6) 1 (5.6) 0 (0.0) 2 (11.1) 16 (88.9) 0.00 94.92 4.73 0.35 0.00 11 (61.1 2 (11.1) 5 (27.8) 0 (0.0) 0 (0.0) 0 (0.0) 90 0 (0.0) 18 (100.0) 18 (100.0) 0 (0.0) 0 (0.0)
18 (100.0) 0 (0.0) 17 (94.4) 1 (5.6) 0 (0.0) 0 (0.0) 0 (0.0) 17 (94.4) 1(5.6) 0 (0.0) 0 (0.0) 0 (0.0) 18 (100.0) 0 (0.0) 0.00 100.00 0.00 0.00 0.00 0 (0.0) 0 (0.0) 18 (100.0) 0 (0.0) 0 (0.0) 0 (0.0) 65 0 (0.0) 18(100.0) 18 (100.0) 0 (0.0) 0 (0.0)
Age of pastoralist
Pastoralist education level
Way of living
Proportion of household income
Livestock enterprise
Average flock size Feeding/browse area Treatment of sick goats
phosphate-buffered saline (PBS) and developed for optical density (OD) reading at 405 nm in an ELISA reader. Optical density values of over 50% were considered positive.
Lemeshow goodness of fit test and the Cox and Snell and Nagelkerke R square values which provided indication of the amount of variation in the independent variable explained by the fitted model.
2.5. Data analysis
3. Results
Questionnaire and serology data were entered in Microsoft Excel spreadsheet. Statistical analyses were carried out using the IBM SPSS statistics 20 software. Odds ratios (OR) and 95% confidence levels (CIs) were calculated to measure the association of the potential risk factors and prevalence of CCPP using binary logistic regression. Univariate models were first run to assess the association between CCPP sero-prevalence and potential risk factors. The risk factors assessed were sex, age, county, location, flock size, source of introductions to the flock, water source, grazing area, season, access to veterinary drugs/services, vaccination status and previous exposure of goats to CCPP. The significance level was set at p < 0.10 based on the likelihood ratio test. A multivariate logistic regression model was subsequently built using significant variables in the univariate analysis. Model building used a stepwise forward method (Hosmer and Lemeshow, 1989) to decide on the factors and significant interactions to include in the model using the likelihood ratio test (P < 0.05). All the significant risk factors were initially included in the model. The strength of association between the risk factor and CCPP sero-positivity was estimated using the odds ratios (OR) which were directly derived from the coefficient estimates from the logistic regression models. Odds ratio is ‘the increase (or decrease if the ratio is less than 1) in odds of being in one outcome category when the value of the predictor increases by one unit’. For each of OR, there is a 95% CI displayed giving a lower and upper value and encompasses the true value of OR and gives confidence that we have in it being an accurate representation of the true value from the population. Model fit was examined using the Hosmer and
A total of 54 flocks from different owners were involved in the study. A summary of the demographic and social structure of the communities that were selected to participate in the study is shown in Table 1. Nomadism and transhumance were the only ways of keeping livestock reported from this study which are typical for pastoral communities. Almost all the respondent pastoralists (98.1%) were males in the age category of 18–35 years, the majority of whom (81.5%) had no formal education and livestock was their main source of livelihood. Rearing of goats was the priority enterprise for the nearly (72.2%) all of the households followed by cattle and sheep in that order. The average herd size per household was 86 goats. Forty nine of the 54 flocks presented at least one seropositive animal giving an overall flock sero-prevalence of 90.7%. Two hundred and four of the 432 goats tested positive by monoclonal antibody based competitive Enzyme-linked immunosorbent assay (c-ELISA) test, hence a sero-prevalence of 47.2% (95% CI = 42.5–51.9). The results of univariate analysis indicated that a number of factors associated with CCPP sero-prevalence. Among the variables, locations, market as source of goats introduced to the flock, sources of water for goats, access to veterinary drugs at distant markets, history of recent vaccination of flocks and previous exposure to CCPP were selected (p < 0.10) for multivariate analysis. Age and sex of the goats were not significantly associated with CCPP sero-prevalence with statistical levels of p = 0.231 and p = 0.107 respectively. Other factors that were not significantly associated with sero-prevalence of the disease were size of the flocks and season of the year (Table 2).
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Table 2 Univariate analysis of factors associated with CCPP sero-prevalence. Variable
Sex Age
County
Location
Flock size
Source of new introductions Source of water
Keeping goats in dry season feeding area Season of the year
Distant access to veterinary drugs Vaccination Previous exposure to CCPP
Category
Male Female weaners Yearling Adults Baringo Turkana Kajiado Kalobeyei Lokichoggio Naudo Oldonyo Orok Orus Torosei 1–100 101–200 201–300 Market Gifts (dowry) River Stream Borehole Dam Shallow well Yes No Wet season Dry season Throughout Distant market Local market Yes No Yes No
No. of goats testing positive
Prevalence (%)
72 132 39 34 131 42 92 70 43 49 16 46 26 24 162 34 8 65 24 17 32 65 26 64 64 140 151 41 11 151 53 32 172 203 1
53.3 44.4 42.4 42.0 50.6 29.2 63.9 48.6 59.7 68.1 22.2 63.9 36.1 33.3 49.4 38.6 50.0 0.58 0.3 21.3 50.0 67.7 36.1 53.3 57.1 43.8 49.8 45.8 41.7 62.9 27.6 66.7 44.8 48.8 6.2
95% C.I.
P-value
Lower
Upper
44.9 38.8 32.2 31.1 44.5 21.7 56.0 40.4 48.8 57.1 11.3 53.0 25.2 22.4 44.0 28.2 25.5 0.5 0.2 10.8 38.3 58.2 25.1 44.8 47.9 38.3 44.3 34.2 21.6 57.0 21.0 52.6 39.8 44.0 1.8
61.8 50.1 52.6 52.9 56.7 36.6 71.7 56.8 70.6 79.0 33.1 74.8 47.0 44.3 54.8 49.1 74.5 0.7 0.4 31.7 61.7 77.3 47.1 61.9 66.4 49.2 55.4 57.4 61.8 68.9 34.2 80.7 49.8 53.6 30.5
0.107 0.231
<0.001
<0.001
0.196
<0.001 <0.001
0.014 0.646
<0.001 0.004 0.001
Table 3 Multivariate analysis of risk factors associated with CCPP sero-prevalence. Variable

S.E.
Wald
EXP()
95% C.I. for EXP()
p-value
Previous exposure to CCPP 1 = Yes, 0 = No Access of veterinary drugs at distant markets 1 = Distant agro-veterinary shops, 0 = Local market Moving goats to dry season feeding areas 1 = Yes, 0 = No Markets as a source of new introductions into the flock 1 = Market, 0 = Gifts (dowry)
3.966 1.819
1.1 0.3
13.7 36.4
52.8 6.17
6.45 3.41
432 11.1
<0.001 <0.001
1.46
0.3
23.7
4.30
2.39
7.75
<0.001
0.618
0.3
4.6
1.86
1.05
3.27
0.033
N = 432, −2Log-likelihood = 332.062 df 6; p = 0.392.
The final multivariate logistic regression model for CCPP seroprevalence is shown in Table 3. The variables considered as risk factors in the model were; previous exposure of flock to CCPP (p < 0.001, OR = 52.8; CI = 6.45, 432), access of veterinary drugs at distant markets (p < 0.001, OR = 6.17 CI = 3.41, 11.1), movement goats to dry season feeding areas (p < 0.001, OR = 4.31 CI = 2.39, 7.75) and markets as a source of new introductions to the flock (p = 0.033, OR = 1.86 CI = 1.05, 3.27). The final model fitted well (Hosmer and Lemeshow, 1989; 2 = 6.289, p = 0.392). Between 25.1 and 33.8% variability was explained by the set of variables as indicated by Cox and Snell and Nagelkerke R square values. There were no significant interactions in the model. 4. Discussion The general characteristics of the study population were typical of an extensive pastoral production system where nomadism and transhumance were practiced by 53.7% and 46.3% of the pastoral-
ists respectively. These traditional livestock production systems are common in most African countries and enhances the spread of CCPP as animals congregate during grazing and watering (Lefevre et al., 1987) given that the disease is highly contagious and infectious and is transmitted by direct contact through inhalation of infective aerosols from infected goats by susceptible goats. In the current study, almost all the flocks (90.7%) presented at least one CCPP sero-positive animal which together with the high regional animal sero-prevalence of 47.2% (95% CI = 42.5–51.9), confirm the endemic state of the disease in the region. The findings were consistent with the results obtained by Peyraud et al., 2014 in a similar study that reported between flock CCPP sero-prevalence varying from 6 to 90% in Narok County although the findings from our study were more specific in reference to the timing of our study and the selection of the study areas. There was a variation in CCPP sero-prevalence in the different counties and locations selected in the study. A significantly higher sero-prevalence of 63.9% (95% CI = 56.0–71.7) and 48.6
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(95% CI = 40.4–56.8) was recorded in study areas in Turkana West Sub-county which shares boundaries with South-Sudan to the North-West and Uganda to the West and Kajiado Central Sub county which shares boundary with Tanzania to the West respectively while study areas in Pokot East Sub-counties which are far from international boundaries had a prevalence of 29.2% (95% CI = 21.7–36.6). A similar observation was reported by Wafula (2007) in a study done in the same region using complement fixation test. The results are a pointer to the high risk due to the porous nature of the international borders of the country and hence there is need for cross-border harmonization of disease control programs including routine vaccination among the neighbouring pastoral communities for effective management of CCPP outbreaks and spread. In this study, none of the animal level variables; sex and age of goats were significantly associated with CCPP sero-positivity in this study. The observation agrees with the reports by Mekuria and Asmare (2010), Eshetu et al. (2007) and OIE (2014) which concluded the above factors to have no role in CCPP epidemiology. However, the results were contradictory to the findings by Mohammed (2008) and Regassa et al. (2010) that reported significant sex difference in CCPP sero-prevalence and a study by Matios et al. (2014) which reported a significantly higher prevalence in the old age category. This may be due to older animals having been at risk of exposure for a longer period than young animals and not necessarily as a result of recent infection. The association of history of exposure of flock to CCPP was expected. Infected goats remain carriers even when treated with the available antibiotics and are a potential risk to the healthy goats in the flock and those they come in contact at feeding areas, watering points and markets. Goats that were purchased from markets were about 2 times more likely to be sero-positive to the disease than the ones offered to households as gifts and dowry. Normally, goats with chronic illness some of which might be infected with CCPP are candidates for culling and most of them are sold in local markets. The disease is commonly spread by direct contact (aerogenic route, through droplets released during coughing) and a very short period of intimate contact is sufficient to transmit the disease (Thiaucourt and Bolske, 1996). A single surviving seropositive goat from a natural outbreak in Thrace region of Turkey for example, was able to infect all 10 disease-free contacts within 2 weeks when kept in close confinement (Ozdemir et al., 2005). Coincidentally, results from the current study showed a strong association between serological prevalence and movement of goats to dry season feeding areas. The recurrent drought episodes commonly experienced in most pastoral regions of the country is a reason for movement of flocks to dry season feeding areas in search of adequate browse and water for goats resulting in a high rate of contact of flocks. The phenomenon has been reported to be ideal for the transmission of CCPP (Seifert, 1996). Cross-border movements were commonly reported in study areas in Turkana West and Kajiado Central which were very remote and as such, the pastoralists had never been visited by veterinary extension officers who are expected to implement the disease control policy. Difficulty in accessing veterinary health services remain a challenge to improving productivity of livestock enterprises pastoral areas. In this study, there was a risk of CCPP sero-prevalence with access to drugs from distant markets. Goats from flocks whose owners could not easily access veterinary drug outlets were 6 times more likely to be sero-positive than those within a close range of distances (less than 20 kilometers) from the veterinary service providers. Most villages in the study areas were beyond this radius (up to 100 Kilometers away) in hilly terrains and transport was unavailable. Moreover, there were frequent reports of insecurity in some areas that were consequently shunned by veterinary ser-
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vice providers (Kipronoh et al., 2016). As a result, treatment of sick animals were delayed and chances of recovery was low. Majority of the pastoralists made their own diagnoses of diseased goats and administered drug combinations that they thought were appropriate. In some areas of Baringo County for example, the pastoralists relied on traditional herbal concoctions whose efficacy against CCPP is unknown. In most cases, sick goats were not promptly or properly treated which could be reason for development of carrier states that plays an important role in the transmission of the disease. The findings are in agreement with a previous report by Sori (1999) which indicated that the impact of insufficient veterinary services in mobile livestock production systems increases the spread of diseases. 5. Conclusion The study provided information on risk factors associated with occurrence of CCPP in goats and further evidence to support the high prevalence and endemic state of the disease in Kenya. The findings suggest that the pastoral flocks are at risk of infection with CCPP due to previous exposure of flocks to CCPP, difficulty in accessing veterinary drugs, movement of goats to dry season feeding areas and introduction of goats into flocks from markets. The above risk factors were found to be significantly associated with CCPP sero-positivity. Consequently there is a need for adequate and coordinated measures to be put in place to control the disease effectively for improved productivity of the goat enterprise in the country. Acknowledgement The study was jointly supported through funding from the Kenya Agricultural and Livestock Research Organization (KALRO) through KAPAP PhD Scholarship grant-KARI/3/047/48 and Kenya’s National Commission of Science, Technology and Innovation (NACOSTI) through NACOSTI/RCD/5TH CALL PhD/001 grant. The authors gratefully acknowledge all the pastoralists and village/adakaar leaders who participated in the study for their maximum cooperation in getting samples for serology. We also appreciate the effort made by the Sub county veterinary officers and their field staff in facilitating the administration of questionnaires and sample collection. References AU-IBAR, 2014. Pan African Animal Health Yearbook 2014. Pan African Animal Health Yearbook, 2014 (accessed 04.03.2016) http://www.au-ibar.org/panafrican-animal-resources-yearbook. AU-IBAR, 2015. Standard Methods and Procedures (SMPs) for Contagious Caprine Pleuropneumonia (CCPP) in the Greater Horn of Africa, Nairobi (accessed 04.03.2016) http://www.au-ibar.org/component/jdownloads/viewdownload/ 76-tmt/2417-tmt-20151218-smp-ccpp-en. Eshetu, L., Yigezu, L., Asfaw, Y., 2007. A study on contagious caprine pleuropneumonia (CCPP) in goats at an export oriented abattoir Debrezeit, Ethiopia. Trop. Anim. Health Prod. 39, 427–432. Hosmer, D.W., Lemeshow, S., 1989. Applied Logistic Regression. Wiley, NewYork. Kipronoh, K.A., Kiara, H.K., Binepal, Y.S., Thuranira, E., Ombui, J.N., 2016. Pastoralists’ perception of constraints affecting goat production in the Rift Valley region of Kenya. Livestock Research for Rural Development. 28, Article #33. http://www.lrrd.org/lrrd28/3/kipr28033.html (accessed 02.03.2016). Lefevre, P.C., Jone, G.E., Ojo, M.O., 1987. Pulmonary mycoplasmosis of small ruminants revue scientifique et technique. Office Int. des ëpizooties 6 (3), 759–799. Manso-Silván, L., Perrier, X., Thiaucourt, F., 2007. Phylogeny of the Mycoplasma mycoides cluster based on analysis of five conserved protein-coding sequences and possible implications for the taxonomy of the group. Int. J. Syst. Evol. Microbiol. 57 (Pt. 10), 2247–2258, 10. Martin, S.W., Meek, A.H., Willeberg, P., 1987. Veterinary Epidemiology Principles and Methods. Iowa State University Press, Ames Iowa (343 pp.). Matios, L., Tesfaye, S., Gelagay, A., Eyop, E., Gebremikael, D., Tadele, T., 2014. Seroprevelence of contagious caprine pleuropneumonia and field performance
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