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Prevalence and incidence of tick-borne diseases in smallholder farming systems in the western-Kenya highlands
Veterinary Parasitology 141 (2006) 307–312 www.elsevier.com/locate/vetpar
Prevalence and incidence of tick-borne diseases in smallholder farming systems in the western-Kenya highlands O.S. Okuthe a,b,*, G.E. Buyu c a
National Veterinary Research Centre, Kenya Agricultural Research Institute (NVRC-KARI), PO Box 32, Kikuyu, Kenya b Terra Nuova, Eastern Africa, PO Box 74916, 00200 Nairobi, Kenya c International Livestock Research Institute, PO Box 30028, Nairobi, Kenya Received 2 September 2005; received in revised form 9 May 2006; accepted 15 May 2006
Abstract The prevalence and incidences of tick-borne diseases (TBDs) infections in cattle were studied in the western-Kenya highlands. Serological tests, thick-blood and lymph-node smears were used to quantify TBDs during cross-sectional and longitudinal studies. Four hundred and eight and 192 (wet season) and 114 and 46 (dry season) cattle were bled for serology in the rural and peri-urban areas, respectively. Seroprevalences differed significantly between the two areas ( p < 0.05). The cattle were monitored for 23 months (259,923 and 126,273 cattle days in the rural and peri-urban areas, respectively) from September 1996 to August 1998. The incidences of babesiosis, anaplasmosis and theileriosis were 0.42%, 4.64% and 4.92% and 1.45%, 32.11% and 39.05% in the rural and peri-urban areas, respectively. The difference in the incidence were significantly different for anaplasmosis and theileriosis ( p < 0.05). The difference in disease frequencies in two areas in close proximity shows the importance of monitoring disease events in order to understand and advice farmers in different production and farming systems appropriately. # 2006 Elsevier B.V. All rights reserved. Keywords: Cattle parasitological disease; Prevalence and incidence; Smallholder farming system; Tick-borne diseases; Kenya highlands
1. Introduction Tick-borne diseases (TBDs) are most prevalent and numerous and exert their greatest impact in the tropical and sub-tropical regions (Bram, 1983, Minjauw and Mcleod, 2003). Theileriosis alone was estimated to cause a loss of US$168 million in 11 African countries in 1989
Abbreviations: ELISA, enzyme linked immunosorbent assay; NVRC, National Veterinary Research Centre; PU, peri-urban area; TBDs, tick-borne diseases; RA, rural area; VIL, Veterinary Investigation Laboratory * Corresponding author. Tel.: +254 20 4445511/722379401; fax: +254 20 4443748. E-mail addresses: [email protected], [email protected] (O.S. Okuthe). 0304-4017/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2006.05.016
(Mukhebi, 1992). Tick-borne diseases caused by Theileria parva, Anaplasma marginale and Babesia bovis are considered to be the most important constraints in the Kenya highlands (Norval et al., 1992; Peeler and Omore, 1997). Estimation of disease frequencies at population level can be used to compare different populations in order to express specific numbers relative to each population. Most of the past epidemiological evaluations of TBDs conducted in Kenya have been on passive data that cannot be extrapolated to other areas. The inadequacy of appropriate data leads to lack of quantification of economic losses from ticks and TBDs and their impacts on livestock productivity (Mukhebi, 1992; Pegram et al., 1989). In the recent past, properly designed epidemiological studies were conducted in various parts of the country
308
O.S. Okuthe, G.E. Buyu / Veterinary Parasitology 141 (2006) 307–312
(Gitau, 1992; O’Callaghan, 1998; Maloo et al., 2001a,b) that gave dependable assessment of risk of TBDs in those areas. This type of studies had not been conducted in the western-Kenya highlands (Wilsmore, 1994). We undertook one as part of a broad study on the assessment of livestock productivity constraints in smallholder farming systems in the western-Kenya highlands (Okuthe, 1999; Okuthe et al., 2003). 2. Materials and methods 2.1. Study area The study was conducted in Uasin Gishu district in the northern part of the Rift Valley province, Kenya. The district lies between 348500 E and 358030 E and 08030 N and 08550 N and is situated in a plateau ranging in altitude from 1900 to 2700 m, running approximately from Northwest to Southeast. Maximum temperatures range from 19 to 24 and minimum temperatures from 13 to 16 8C. The district has a highland-equatorial type of climate with a mean annual rainfall of 1124 mm which is a weakly bimodal pattern, with peaks occurring in April and August (Jaetzold and Schimdt, 1983). 2.2. Study design The cross-sectional study was conducted in 60 farms both in the rural (RA) and peri-urban (PU) areas. The farms were selected using a three-stage random procedure. The first stage involved a random selection of a sub-location (smaller unit of a district) from the two sites. The second stage involved a random selection of two villages from each of the selected sub-location. All farms within the villages were listed. Thirty farms from each village then were selected randomly. The crosssectional serological survey was carried out to quantify the prevalence of the three main infections (theileriosis, anaplasmosis and babesiosis) in September 1996 (rainy season) and February 1997 (dry season). The longitudinal study was conducted within the same farms. The occurrence of clinical cases of TBDs was evaluated for a period of 23 months from the 1st September 1996 to 31st July 1998. Two technicians, one at each site collected all the information. The technicians are veterinary assistants trained for 2 years (certificate level) and can diagnose diseases both clinically and by laboratory confirmation. The technicians visited each of the farms twice per month. The senior author visited each farm once per month. Data were obtained by the use of questionnaires and direct observation. Tick control methods, their frequency of application and
brand of drugs used, were also recorded. For accurate identification each cow was ear tagged with a number representing the location, farm and individual animal. 2.3. Testing for serum antibodies The cross-sectional survey was done in all farms keeping cattle. Cattle in 60 and 59 farms were bled in the rural and the peri-urban areas, respectively. Six hundred cattle were bled (408 rural and 192 peri-urban) during the wet season (September). One hundred and sixty cattle (114 rural and 46 peri-urban) were bled in the dry season (February) in a sub-sample of the study farms randomly selected. Blood for serum preparation was taken from all the cattle in the farms in each visit in the wet season. During the dry season cattle were sampled in 10 randomly selected farms from each village. Blood was collected from each animal by jugular venipuncture using 10-ml vacutainer tubes (Becton Dickson Vacutainer Systems, England). The principal author verified correct labelling of the tubes. Blood was then kept in cool boxes with ice for about 5 h. The blood samples were refrigerated at the end of the day in the local Veterinary Investigation Laboratory (VIL) in Eldoret town (district headquarters). The blood was centrifuged at 3000 g for 20 min in the laboratory. Two aliquots of sera, each approximately 1 ml, were made from each sample and stored in a freezer at 20 8C until the tests were done. The enzyme-linked-immunosorbent assay (ELISA) as described by Katende et al. (1996) estimated seasonspecific, area specific infection prevalences to the three main TBDs (theileriosis, anaplasmosis and babesiosis) identified in the first phase of the study (Okuthe et al., 1997). The serology work was done at the National Veterinary Research Centre (NVRC) laboratories (Muguga), 33 kms from Nairobi where the principal author is based. 2.4. Evaluation of incidence of tick-borne diseases During the 23-month longitudinal study, all suspect clinical cases of TBDs were confirmed by taking the appropriate sample. Blood smears were taken for each suspect case of any of the three TBDs. Lymph-node biopsy smears also were taken for any suspect case of theileriosis because this is the most-effective method available to date for parasite detection (Norval et al., 1991). The smears were fixed in alcohol for 5 min before being taken to the regional VIL for staining and smear examination. The presence of piroplasms and macroschizonts were confirmatory for theileriosis. The
O.S. Okuthe, G.E. Buyu / Veterinary Parasitology 141 (2006) 307–312
results were recorded in hard cover field notebooks and later entered into disease incidence forms. Incidence was calculated as true rates (Putt et al., 1987), based on cattle days contributed by each animal during the observation period. The true incidence rates were calculated by dividing the number of confirmed disease cases by total cattle days and multiplying by 365 and 100 to get the cattleyear percentage rate. 2.5. Data entry and statistical analysis Disease incidence was entered in the Microsoft Access programme in pre-prepared files immediately after the serological tests. The data were crosschecked with the field-notebook raw data. The statistical analysis was done using Microsoft Excel for Windows (Version 4.0), STATISTIX (Version 4.0, Analytical Software, St. Paul, MN) and Epi Info (Version 6.02, Centre for Disease Control, Atlanta, GA). Pearson’s Chi-square tests were used to compare the seroprevalences and specific disease incidences. Statistical significance was tested at the 95% confidence level.
309
Table 2 Tick control and management practices in the rural and peri-urban areas of Uasin Gishu District, Kenya. Longitudinal study (September 1996–July 1998) Grazing/tick control
Rural (%)
Peri-urban (%)
Type of grazing Zero Semi-zero Paddocked Communal
0 0 26.6 73.4
2.40 28.30 9.60 59.70
Tick control per month (times) <1 5.40 2 2.30 3 0.10 4 92.20
3.80 2.00 0 94.20
Acaricide brand Triatix Steladone Delnav
98.90 1.20 0
97.60 0 2.40
Tick control method Dipping Hand spray Hand wash
6.30 92.90 0.8
2.00 97.2 0.8
1 Triatix_(Cooper Kenya Ltd.) is an amidine based acaricide. 2 Steladone_(Kenya Swiss Ltd.) is a Chlorfenvinphos based acaricide. 3 Delnav DFF_(Cooper Kenya Ltd.) is an organophosphate based acaricide.
3. Results 3.1. Herd structure, management practices and tick-borne diseases control There were relatively more calves and adults in the RA than the PU area. This pattern was reversed in weaners (Table 1) that also give other descriptive statistics on cattle numbers. The cow: bull ratio was 25 and 53 for the RA and PU areas, respectively. The main type of grazing in the RA (73.4%) and PU (59.7%) areas was communal (Table 2). The major tick control frequency, acaricide brand and tick control in the RA and PU areas was four times per month, TriatixR and hand spray. Detail of other Table 1 Mean herd proportions (%) of cattle by age and sex in the rural and peri-urban areas of Uasin Gishu District, Kenya (September 1996– July 1998) Category
Rural
Peri-urban
minor proportions for the same management practices is shown in Table 2. In the longitudinal studies, tick control was irregular in 10% and 35% of the farms in the RA and PU areas, respectively. Five and 20% of the farmers who applied acaricides irregularly used under strength solutions (RA and PU areas, respectively) as did 23% and 27% of the farmers who regularly controlled ticks. In the RA, mixing and preparation of acaricides was mostly done by the farmer himself (97%) compared to 75% in the PU area (the other 25% of tick control was being managed by farm workers). Farmers attributed the irregular tick control and the use of under-strength acaricide to lack
Table 3 Comparison of the seroprevalence of tick-borne disease pathogens in the rural and peri-urban areas of Uasin Gishu district, Kenya (September 1996)
Male
Female
Male
Female
Rural area
Calves Weaners Adults
14.75 9.01 2.17
13.88 6.66 53.52
9.46 7.34 0.97
13.70 16.70 51.83
Number Percentage
Whole herd
100.00
100.00
Theileriosis 234 Anaplasmosis 203 Babesiosis 152
59.7 50.2 37.1
p-Value Peri-urban area Number Percentage 0.001 0.001 0.02
142 62 53
73.2 32.1 27.5
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Table 4 Animal days, cases and incidences of tick-borne diseases in Uasin Gishu District from a longitudinal observational study (September 1996–July 1998)
Cattle days
Rural area
p-Value
Peri-urban area
259923
NA
126273
Confirmed cases (incidence) Theileriosis 35 (4.9%) Anaplasmosis 33 (4.6%) Babesiosis 3 (0.4%)
0.001 0.001 0.07
131 (39.1%) 111 (32.1%) 5 (1.5%)
NA, not applicable.
of cash as a result of poor milk-marketing facilities and irregular payments. 3.2. Prevalence of tick-borne diseases The prevalence of TBDs was higher during the rainy season than the dry season in the UM compared to the PU where it was higher in the dry season than the wet season. Table 3 shows the comparison of seroprevalence of TBDs in the two areas. There were significant differences in the prevalence rate of TBDs ( p < 0.05) between the two areas. 3.3. Incidence of tick-borne diseases The incidence of TBDs was higher in the peri-urban area than in the rural area (Table 4). Table 4 shows that the incidence of theileriosis and anaplasmosis in the two areas was significantly different ( p < 0.05). This follows the same pattern as for disease prevalence. 4. Discussion Treatment of all TBDs during the study acted as an incentive for efficient reporting of disease cases. Hence the high quality of the data obtained in this study on TBDs incidence. The higher prevalence and incidence of TBDs in the peri-urban than the rural area could be attributed to three factors. The first factor was the relatively higher proportion of irregular tick control in the peri-urban compared to the rural area. The personnel who were responsible for the management of tick control also aggravated this situation. In the peri-urban, farm workers who might not constitute the acaricide solutions to effective standards did about 25% compared to 3.3% in the rural area of tick control management. The second factor is that farmers in the rural area prioritised livestock rearing more highly than the peri-urban area. Most farmers in the rural area
depended entirely on crop and livestock farming for their up keep compared to the peri-urban farmers who had other sources of income (employment and business). The third factor is the grazing practices in the two areas, which might influence tick infestation between animals. The communal grazing lands are different between the two areas. In the rural area, there were more communal grazing lands (roadsides, cattle watering points and forests) compared to the peri-urban area where all the cattle had access to only one communal grazing field. In the rural area, farmers took care of their animals individually and therefore close interaction between herds was not a common feature. In the peri-urban area, one herder (paid on a monthly basis could graze from 10 to 20 herds). This practice could promote tick infestation between individual animals and herds especially where relatively poor tick control was practised. Hence, we suspect that the risk of disease transmission risk was higher in the PU area. Most farmers in the PU graze their animals in communal grazing grounds because of lack of pasture on their farms, which mostly were devoted to crop farming. Ticks are easily spread in communal grazing grounds. This agrees with earlier reports (ROK, 1996) that documented under-strength dip samples from various community dips in Kenya. Also, tick-control practices in the rural area was more regular (and hence apparently more effective) than in the PA area. 5. Conclusions This study has shows that the incidence and prevalence of TBDs is high amongst resource poor smallholder dairy farming system in the western-Kenya highlands. This is the first epidemiological study that has quantified the risk of TBDs in the western-Kenya highlands using a longitudinal observational study. Other studies that include Gitau (1992) and Maloo (1993) only depicted that TBDs were the major causes of deaths in dairy cattle production systems in the central Kenya highlands and the coast regions, respectively. The results compares well with other studies conducted in other areas of Kenya within the same production system. The prevalence and incidence of TBDs fall within the range of other studies carried out by Latif et al. (1994), Gitau et al. (1997), Gitau et al. (1999, 2000) and Maloo et al. (2001a,b). These findings agree with qualitative surveys carried out earlier before the observational study (Okuthe et al., 1997; Okuthe et al., 2003). Poor tick control could be a drawback to the development of dairy-cattle production as it agrees with earlier reports (ROK, 1996) that documented under
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strength dip samples from various community dips in Kenya. The study also shows the importance of assessing the epidemiological status of the major TBDs in different production systems, as the incidences were significantly different between different management systems that were in close proximity. The quantification of TBDs in this study would be used in prioritisation of animal health research in the smallholder production system. These findings could also be applied in the evaluation of national economic losses due to TBDs in Kenya as advocated by Peeler and Omore (1997) and Henken et al. (1999). Consequently, the findings of this study as important information that should be disseminated and could also be used in planning and monitoring tick control programmes in smallholder farming systems. Acknowledgements We acknowledge the Department for International Development (DFID) and Kenya Agricultural Research Institute (KARI) for the financial support. The Ministry of Agriculture Livestock Development and Marketing is also acknowledged for the co-operation and logistic support. We highly appreciate and feel indebted to the wonderful smallholder farmers in Uasin Gishu district for their co-operation and understanding during the study period. References Bram, R.A., 1983. Tick-borne livestock diseases and their vectors: the global problem. In: Ticks and Tick-borne Diseases, FAO Animal Production and Health Paper No. 36. Food and Agricultural Organisation, Rome, pp. 7–11. Gitau, G.K., 1992. Health and productivity of calves in smallholder dairy farms in Kiambu district, Kenya. MSc Thesis. University of Nairobi. Gitau, G.K., McDermott, J.J., Katende, J.M., O’Callagan, C.J., Brown, R., Perry, B.D., 2000. Differences in the epidemiology of theileriosis in contrasting agro-ecological and grazing strata of highland Kenya. Epidemiol. Infect. 124, 325–335. Gitau, G.K., Perry, B.P., Katende, J.M., Mcdermott, J.J., Morzaria, S.P., Young, A.S., 1997. The prevalence of serum antibodies to tick-borne infections of cattle in smallholder dairy farms in Murang’a District, Kenya; a cross-sectional study. Prev. Vet. Med. 30, 95–107. Gitau, G.K., Perry, B.D., McDermott, J.J., 1999. The incidence, calf morbidity and mortality due to Theileria parva infections in smallholder dairy farms in Murang’a District, Kenya. Prevent. Vet. Med. 39, 65–79. Henken, A.M., Graat, E.A.M., Casal, J., 1999. Measurement of disease frequency. In: Noordhuizen, J.P.T.M., Frankena, K., van der Hoofd, C.M.,Graat, E.A.M. (Eds.), Application of Quantitative Methods in Veterinary Epidemiology. pp. 65–97.
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Jaetzold, R., Schimdt, H., 1983. Farm management Handbook of Kenya, vol. II.B. Ministry of Agriculture, Central Kenya, Nairobi. Katende, J.M., Morzaria, Toye, S.P., Skilton, R., Nene, V., Morzaria, S.P., Musoke, A.J., 1996. An ELISA for detection of Theileria parva antibodies in cattle using a recombinant polymorphic immunodominant molecule. Parasitol. Res. 84, 408–416. Latif, A.A., Rowlands, G.J., Punyua, D.K., Hassan, S.M., Capstick, P.B., 1994. An epidemiological study of tick-borne diseases and their effects on productivity of zebu cattle under traditional management on Rusinga Island, western Kenya. Prevent. Vet. Med. 22, 169–181. Maloo, S.H., 1993. Epidemiological study of vector-borne diseases with consequent development of preventive medicine programmes for smallholder dairy farmers in coastal Kenya. PhD Thesis. University of Glasgow, UK. Maloo, S.H., Thorpe, W., Kioo, G., Ngumi, Rowlands, G.J., Perry, B.D., 2001a. Sero-prevalencee of vector-transmitted infections of small-holder dairy cattle in coastal Kenya. Prevent. Vet. Med. 52, 1–16. Maloo, S.H., Rowlands, G.J., Thorpe, W., Gettinby, G., Perry, B.D., 2001b. A longitudinal study of disease incidence and case-fatality risks on small-holder dairy farms I coastal Kenya. Prevent. Vet. Med. 52, 17–29. Minjauw, B., Mcleod, A., 2003. Tick-borne diseases and poverty. The impact of ticks and tick-borne diseases on the livelihoods of smallscale and marginal livestock owners in India and eastern and southern Africa. Research report, DFID Animal Health Programme, Centre for Tropical Veterinary Medicine, University of Edinburgh, UK. Mukhebi, A.W., 1992. The economic impact of theileriosis and its control in Africa. In: Norval, R.A.I., Perry, B.D., Young, A.S. (Eds.), The Epidemiology of Theileriosis in Africa. Academic Press, Harcourt Brace Jovanovich, Publishers, pp. 380–402. Norval, R.A.I., Perry, B.D., Gebreab, F., Lessard, 1991. East Coast fever: a problem of the future for the horn of Africa? Prev. Vet. Med. 10, 163–172. Norval, R.A.I., Perry, B.D., Young, A.S., 1992. The Epidemiology of Theileriosis in Africa. Academic Press, Harcourt Brace Jovanovich, Publishers, pp. 236–253. O’Callaghan, C., 1998. A study of the epidemiology of theileriosis of smallholder dairy farmers in Kiambu district, Kenya. PhD Thesis. Faculty of graduate studies, University of Guelph, Canada. Okuthe, O.S., 1999. Participatory Epidemiological Assessment of Livestock Productivity Constraints in the western Kenya Highlands. PhD Thesis. The University of Reading. Okuthe, O.S., Otte, J., Mcleod, A., Peeler, E.J., Omore, A.O., 1997. Assessment of livestock constraints in the smallholder mixed farming systems in the western Kenya highlands. In:Proceedings of the Eighth International Symposium for Veterinary Epidemiology and Economics (ISVEE), 7–11 July, 1997, Paris, France, Epidemiologie Sante Anemale 31–32, p2.08. Okuthe, O.S., MCleod, A., Otte, M.J., Buyu, G.E., 2003. Use of rapid rural appraisal and cross-sectional studies in the assessment of constraints in smallholder cattle production systems in the western Kenya highlands. Onderstepoort J. Vet. Res. 70, 237–242. Peeler, E.J., Omore, A., 1997. Manual of Livestock Production Systems in Kenya, 2nd ed. Pegram, R.G., Lemche, J., Chizyuka, H.J.B., Sutherst, R.W., Floyd, R.B., Kerr, J.D., Mccosker, P.J., 1989. Effects of tick control of
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liveweight gain of cattle in central Zambia. Vet. Med. Entomol. 3, 313–320. Putt, S.N.H., Shaw, A.P.M., Woods, A.J., Taylor, L., James, A.D., 1987. Veterinary Epidemiology and Economics in Africa. A manual for Use in the Design and Appraisal of Livestock Health Policy. ILCA Manual No. 3. VEERU, Department of Agriculture, University of Reading, Reading England.
ROK, 1996. Republic of Kenya. Ministry of Agriculture and Livestock Development, Department of Livestock Production. Annual Report. Wilsmore, A.J., 1994. Kenya National Agricultural Research Project, Second Phase (NARP II), Socio-economics and epidemiology project. Second report of the consultant veterinary epidemiologist.
Prevalence and incidence of tick-borne diseases in smallholder farming systems in the western-Kenya highlands O.S. Okuthe a,b,*, G.E. Buyu c a
National Veterinary Research Centre, Kenya Agricultural Research Institute (NVRC-KARI), PO Box 32, Kikuyu, Kenya b Terra Nuova, Eastern Africa, PO Box 74916, 00200 Nairobi, Kenya c International Livestock Research Institute, PO Box 30028, Nairobi, Kenya Received 2 September 2005; received in revised form 9 May 2006; accepted 15 May 2006
Abstract The prevalence and incidences of tick-borne diseases (TBDs) infections in cattle were studied in the western-Kenya highlands. Serological tests, thick-blood and lymph-node smears were used to quantify TBDs during cross-sectional and longitudinal studies. Four hundred and eight and 192 (wet season) and 114 and 46 (dry season) cattle were bled for serology in the rural and peri-urban areas, respectively. Seroprevalences differed significantly between the two areas ( p < 0.05). The cattle were monitored for 23 months (259,923 and 126,273 cattle days in the rural and peri-urban areas, respectively) from September 1996 to August 1998. The incidences of babesiosis, anaplasmosis and theileriosis were 0.42%, 4.64% and 4.92% and 1.45%, 32.11% and 39.05% in the rural and peri-urban areas, respectively. The difference in the incidence were significantly different for anaplasmosis and theileriosis ( p < 0.05). The difference in disease frequencies in two areas in close proximity shows the importance of monitoring disease events in order to understand and advice farmers in different production and farming systems appropriately. # 2006 Elsevier B.V. All rights reserved. Keywords: Cattle parasitological disease; Prevalence and incidence; Smallholder farming system; Tick-borne diseases; Kenya highlands
1. Introduction Tick-borne diseases (TBDs) are most prevalent and numerous and exert their greatest impact in the tropical and sub-tropical regions (Bram, 1983, Minjauw and Mcleod, 2003). Theileriosis alone was estimated to cause a loss of US$168 million in 11 African countries in 1989
Abbreviations: ELISA, enzyme linked immunosorbent assay; NVRC, National Veterinary Research Centre; PU, peri-urban area; TBDs, tick-borne diseases; RA, rural area; VIL, Veterinary Investigation Laboratory * Corresponding author. Tel.: +254 20 4445511/722379401; fax: +254 20 4443748. E-mail addresses: [email protected], [email protected] (O.S. Okuthe). 0304-4017/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2006.05.016
(Mukhebi, 1992). Tick-borne diseases caused by Theileria parva, Anaplasma marginale and Babesia bovis are considered to be the most important constraints in the Kenya highlands (Norval et al., 1992; Peeler and Omore, 1997). Estimation of disease frequencies at population level can be used to compare different populations in order to express specific numbers relative to each population. Most of the past epidemiological evaluations of TBDs conducted in Kenya have been on passive data that cannot be extrapolated to other areas. The inadequacy of appropriate data leads to lack of quantification of economic losses from ticks and TBDs and their impacts on livestock productivity (Mukhebi, 1992; Pegram et al., 1989). In the recent past, properly designed epidemiological studies were conducted in various parts of the country
308
O.S. Okuthe, G.E. Buyu / Veterinary Parasitology 141 (2006) 307–312
(Gitau, 1992; O’Callaghan, 1998; Maloo et al., 2001a,b) that gave dependable assessment of risk of TBDs in those areas. This type of studies had not been conducted in the western-Kenya highlands (Wilsmore, 1994). We undertook one as part of a broad study on the assessment of livestock productivity constraints in smallholder farming systems in the western-Kenya highlands (Okuthe, 1999; Okuthe et al., 2003). 2. Materials and methods 2.1. Study area The study was conducted in Uasin Gishu district in the northern part of the Rift Valley province, Kenya. The district lies between 348500 E and 358030 E and 08030 N and 08550 N and is situated in a plateau ranging in altitude from 1900 to 2700 m, running approximately from Northwest to Southeast. Maximum temperatures range from 19 to 24 and minimum temperatures from 13 to 16 8C. The district has a highland-equatorial type of climate with a mean annual rainfall of 1124 mm which is a weakly bimodal pattern, with peaks occurring in April and August (Jaetzold and Schimdt, 1983). 2.2. Study design The cross-sectional study was conducted in 60 farms both in the rural (RA) and peri-urban (PU) areas. The farms were selected using a three-stage random procedure. The first stage involved a random selection of a sub-location (smaller unit of a district) from the two sites. The second stage involved a random selection of two villages from each of the selected sub-location. All farms within the villages were listed. Thirty farms from each village then were selected randomly. The crosssectional serological survey was carried out to quantify the prevalence of the three main infections (theileriosis, anaplasmosis and babesiosis) in September 1996 (rainy season) and February 1997 (dry season). The longitudinal study was conducted within the same farms. The occurrence of clinical cases of TBDs was evaluated for a period of 23 months from the 1st September 1996 to 31st July 1998. Two technicians, one at each site collected all the information. The technicians are veterinary assistants trained for 2 years (certificate level) and can diagnose diseases both clinically and by laboratory confirmation. The technicians visited each of the farms twice per month. The senior author visited each farm once per month. Data were obtained by the use of questionnaires and direct observation. Tick control methods, their frequency of application and
brand of drugs used, were also recorded. For accurate identification each cow was ear tagged with a number representing the location, farm and individual animal. 2.3. Testing for serum antibodies The cross-sectional survey was done in all farms keeping cattle. Cattle in 60 and 59 farms were bled in the rural and the peri-urban areas, respectively. Six hundred cattle were bled (408 rural and 192 peri-urban) during the wet season (September). One hundred and sixty cattle (114 rural and 46 peri-urban) were bled in the dry season (February) in a sub-sample of the study farms randomly selected. Blood for serum preparation was taken from all the cattle in the farms in each visit in the wet season. During the dry season cattle were sampled in 10 randomly selected farms from each village. Blood was collected from each animal by jugular venipuncture using 10-ml vacutainer tubes (Becton Dickson Vacutainer Systems, England). The principal author verified correct labelling of the tubes. Blood was then kept in cool boxes with ice for about 5 h. The blood samples were refrigerated at the end of the day in the local Veterinary Investigation Laboratory (VIL) in Eldoret town (district headquarters). The blood was centrifuged at 3000 g for 20 min in the laboratory. Two aliquots of sera, each approximately 1 ml, were made from each sample and stored in a freezer at 20 8C until the tests were done. The enzyme-linked-immunosorbent assay (ELISA) as described by Katende et al. (1996) estimated seasonspecific, area specific infection prevalences to the three main TBDs (theileriosis, anaplasmosis and babesiosis) identified in the first phase of the study (Okuthe et al., 1997). The serology work was done at the National Veterinary Research Centre (NVRC) laboratories (Muguga), 33 kms from Nairobi where the principal author is based. 2.4. Evaluation of incidence of tick-borne diseases During the 23-month longitudinal study, all suspect clinical cases of TBDs were confirmed by taking the appropriate sample. Blood smears were taken for each suspect case of any of the three TBDs. Lymph-node biopsy smears also were taken for any suspect case of theileriosis because this is the most-effective method available to date for parasite detection (Norval et al., 1991). The smears were fixed in alcohol for 5 min before being taken to the regional VIL for staining and smear examination. The presence of piroplasms and macroschizonts were confirmatory for theileriosis. The
O.S. Okuthe, G.E. Buyu / Veterinary Parasitology 141 (2006) 307–312
results were recorded in hard cover field notebooks and later entered into disease incidence forms. Incidence was calculated as true rates (Putt et al., 1987), based on cattle days contributed by each animal during the observation period. The true incidence rates were calculated by dividing the number of confirmed disease cases by total cattle days and multiplying by 365 and 100 to get the cattleyear percentage rate. 2.5. Data entry and statistical analysis Disease incidence was entered in the Microsoft Access programme in pre-prepared files immediately after the serological tests. The data were crosschecked with the field-notebook raw data. The statistical analysis was done using Microsoft Excel for Windows (Version 4.0), STATISTIX (Version 4.0, Analytical Software, St. Paul, MN) and Epi Info (Version 6.02, Centre for Disease Control, Atlanta, GA). Pearson’s Chi-square tests were used to compare the seroprevalences and specific disease incidences. Statistical significance was tested at the 95% confidence level.
309
Table 2 Tick control and management practices in the rural and peri-urban areas of Uasin Gishu District, Kenya. Longitudinal study (September 1996–July 1998) Grazing/tick control
Rural (%)
Peri-urban (%)
Type of grazing Zero Semi-zero Paddocked Communal
0 0 26.6 73.4
2.40 28.30 9.60 59.70
Tick control per month (times) <1 5.40 2 2.30 3 0.10 4 92.20
3.80 2.00 0 94.20
Acaricide brand Triatix Steladone Delnav
98.90 1.20 0
97.60 0 2.40
Tick control method Dipping Hand spray Hand wash
6.30 92.90 0.8
2.00 97.2 0.8
1 Triatix_(Cooper Kenya Ltd.) is an amidine based acaricide. 2 Steladone_(Kenya Swiss Ltd.) is a Chlorfenvinphos based acaricide. 3 Delnav DFF_(Cooper Kenya Ltd.) is an organophosphate based acaricide.
3. Results 3.1. Herd structure, management practices and tick-borne diseases control There were relatively more calves and adults in the RA than the PU area. This pattern was reversed in weaners (Table 1) that also give other descriptive statistics on cattle numbers. The cow: bull ratio was 25 and 53 for the RA and PU areas, respectively. The main type of grazing in the RA (73.4%) and PU (59.7%) areas was communal (Table 2). The major tick control frequency, acaricide brand and tick control in the RA and PU areas was four times per month, TriatixR and hand spray. Detail of other Table 1 Mean herd proportions (%) of cattle by age and sex in the rural and peri-urban areas of Uasin Gishu District, Kenya (September 1996– July 1998) Category
Rural
Peri-urban
minor proportions for the same management practices is shown in Table 2. In the longitudinal studies, tick control was irregular in 10% and 35% of the farms in the RA and PU areas, respectively. Five and 20% of the farmers who applied acaricides irregularly used under strength solutions (RA and PU areas, respectively) as did 23% and 27% of the farmers who regularly controlled ticks. In the RA, mixing and preparation of acaricides was mostly done by the farmer himself (97%) compared to 75% in the PU area (the other 25% of tick control was being managed by farm workers). Farmers attributed the irregular tick control and the use of under-strength acaricide to lack
Table 3 Comparison of the seroprevalence of tick-borne disease pathogens in the rural and peri-urban areas of Uasin Gishu district, Kenya (September 1996)
Male
Female
Male
Female
Rural area
Calves Weaners Adults
14.75 9.01 2.17
13.88 6.66 53.52
9.46 7.34 0.97
13.70 16.70 51.83
Number Percentage
Whole herd
100.00
100.00
Theileriosis 234 Anaplasmosis 203 Babesiosis 152
59.7 50.2 37.1
p-Value Peri-urban area Number Percentage 0.001 0.001 0.02
142 62 53
73.2 32.1 27.5
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Table 4 Animal days, cases and incidences of tick-borne diseases in Uasin Gishu District from a longitudinal observational study (September 1996–July 1998)
Cattle days
Rural area
p-Value
Peri-urban area
259923
NA
126273
Confirmed cases (incidence) Theileriosis 35 (4.9%) Anaplasmosis 33 (4.6%) Babesiosis 3 (0.4%)
0.001 0.001 0.07
131 (39.1%) 111 (32.1%) 5 (1.5%)
NA, not applicable.
of cash as a result of poor milk-marketing facilities and irregular payments. 3.2. Prevalence of tick-borne diseases The prevalence of TBDs was higher during the rainy season than the dry season in the UM compared to the PU where it was higher in the dry season than the wet season. Table 3 shows the comparison of seroprevalence of TBDs in the two areas. There were significant differences in the prevalence rate of TBDs ( p < 0.05) between the two areas. 3.3. Incidence of tick-borne diseases The incidence of TBDs was higher in the peri-urban area than in the rural area (Table 4). Table 4 shows that the incidence of theileriosis and anaplasmosis in the two areas was significantly different ( p < 0.05). This follows the same pattern as for disease prevalence. 4. Discussion Treatment of all TBDs during the study acted as an incentive for efficient reporting of disease cases. Hence the high quality of the data obtained in this study on TBDs incidence. The higher prevalence and incidence of TBDs in the peri-urban than the rural area could be attributed to three factors. The first factor was the relatively higher proportion of irregular tick control in the peri-urban compared to the rural area. The personnel who were responsible for the management of tick control also aggravated this situation. In the peri-urban, farm workers who might not constitute the acaricide solutions to effective standards did about 25% compared to 3.3% in the rural area of tick control management. The second factor is that farmers in the rural area prioritised livestock rearing more highly than the peri-urban area. Most farmers in the rural area
depended entirely on crop and livestock farming for their up keep compared to the peri-urban farmers who had other sources of income (employment and business). The third factor is the grazing practices in the two areas, which might influence tick infestation between animals. The communal grazing lands are different between the two areas. In the rural area, there were more communal grazing lands (roadsides, cattle watering points and forests) compared to the peri-urban area where all the cattle had access to only one communal grazing field. In the rural area, farmers took care of their animals individually and therefore close interaction between herds was not a common feature. In the peri-urban area, one herder (paid on a monthly basis could graze from 10 to 20 herds). This practice could promote tick infestation between individual animals and herds especially where relatively poor tick control was practised. Hence, we suspect that the risk of disease transmission risk was higher in the PU area. Most farmers in the PU graze their animals in communal grazing grounds because of lack of pasture on their farms, which mostly were devoted to crop farming. Ticks are easily spread in communal grazing grounds. This agrees with earlier reports (ROK, 1996) that documented under-strength dip samples from various community dips in Kenya. Also, tick-control practices in the rural area was more regular (and hence apparently more effective) than in the PA area. 5. Conclusions This study has shows that the incidence and prevalence of TBDs is high amongst resource poor smallholder dairy farming system in the western-Kenya highlands. This is the first epidemiological study that has quantified the risk of TBDs in the western-Kenya highlands using a longitudinal observational study. Other studies that include Gitau (1992) and Maloo (1993) only depicted that TBDs were the major causes of deaths in dairy cattle production systems in the central Kenya highlands and the coast regions, respectively. The results compares well with other studies conducted in other areas of Kenya within the same production system. The prevalence and incidence of TBDs fall within the range of other studies carried out by Latif et al. (1994), Gitau et al. (1997), Gitau et al. (1999, 2000) and Maloo et al. (2001a,b). These findings agree with qualitative surveys carried out earlier before the observational study (Okuthe et al., 1997; Okuthe et al., 2003). Poor tick control could be a drawback to the development of dairy-cattle production as it agrees with earlier reports (ROK, 1996) that documented under
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strength dip samples from various community dips in Kenya. The study also shows the importance of assessing the epidemiological status of the major TBDs in different production systems, as the incidences were significantly different between different management systems that were in close proximity. The quantification of TBDs in this study would be used in prioritisation of animal health research in the smallholder production system. These findings could also be applied in the evaluation of national economic losses due to TBDs in Kenya as advocated by Peeler and Omore (1997) and Henken et al. (1999). Consequently, the findings of this study as important information that should be disseminated and could also be used in planning and monitoring tick control programmes in smallholder farming systems. Acknowledgements We acknowledge the Department for International Development (DFID) and Kenya Agricultural Research Institute (KARI) for the financial support. The Ministry of Agriculture Livestock Development and Marketing is also acknowledged for the co-operation and logistic support. We highly appreciate and feel indebted to the wonderful smallholder farmers in Uasin Gishu district for their co-operation and understanding during the study period. References Bram, R.A., 1983. Tick-borne livestock diseases and their vectors: the global problem. In: Ticks and Tick-borne Diseases, FAO Animal Production and Health Paper No. 36. Food and Agricultural Organisation, Rome, pp. 7–11. Gitau, G.K., 1992. Health and productivity of calves in smallholder dairy farms in Kiambu district, Kenya. MSc Thesis. University of Nairobi. Gitau, G.K., McDermott, J.J., Katende, J.M., O’Callagan, C.J., Brown, R., Perry, B.D., 2000. Differences in the epidemiology of theileriosis in contrasting agro-ecological and grazing strata of highland Kenya. Epidemiol. Infect. 124, 325–335. Gitau, G.K., Perry, B.P., Katende, J.M., Mcdermott, J.J., Morzaria, S.P., Young, A.S., 1997. The prevalence of serum antibodies to tick-borne infections of cattle in smallholder dairy farms in Murang’a District, Kenya; a cross-sectional study. Prev. Vet. Med. 30, 95–107. Gitau, G.K., Perry, B.D., McDermott, J.J., 1999. The incidence, calf morbidity and mortality due to Theileria parva infections in smallholder dairy farms in Murang’a District, Kenya. Prevent. Vet. Med. 39, 65–79. Henken, A.M., Graat, E.A.M., Casal, J., 1999. Measurement of disease frequency. In: Noordhuizen, J.P.T.M., Frankena, K., van der Hoofd, C.M.,Graat, E.A.M. (Eds.), Application of Quantitative Methods in Veterinary Epidemiology. pp. 65–97.
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