A cross-sectional survey on fasciolosis in selected settlements of Taveta Division, Coast Province, Kenya

E O Mungube, D M Sila, C W Kariuki, S M Bauni¹, B A Tenhagen², L Wamae³, J Nginyi⁴ and G A Omondi^4,5

Kenya Agricultural Research Institute, Katumani Research Centre, P.O Box 340-90100 Machakos, Kenya
wamateka@hotmail.com
¹Kenya Agricultural Research Institute, Muguga South Research Centre, P.O. Box 30148-00100, Muguga, Kenya
²Bundesinstitut für Risikobewertung, Diedersdorfer Weg 1 D - 12277 Berlin, Tel.: +49-30-18412-0, Fax: +49-(0)30-18412-47/41
³Kenya Agricultural Research Institute, Headquarters, P.O. Box 57811-00200, Nairobi
⁴Kenya Agricultural Research Institute, Veterinary Research Centre, PO Box 32-00902, Kikuyu, Kenya
⁵International Livestock Research Institute (ILRI), Nairobi, P.O. Box 30709-00100, Nairobi Kenya

Abstract

A cross-sectional survey on fasciolosis was conducted in March 2009 in Taveta Division. Bura Ndogo, Challa, Kiwalwa, Kitogoto and Lake Jipe Gicheha settlements participated in the study. A total of 338 (197 cattle, 111 goats and 30 sheep) faecal samples from 42 herds were examined using the sedimentation technique. Similarly, husbandry practices and aspects of herd owner education in the same settlements were captured using a standard questionnaire.  

Selective deworming targeted at the sick and /or weak looking animals was done by some herd owners interviewed. Fasciolosis prevalence in cattle, goats and sheep was 25.9%, 23.4% and 33.3%, respectively. Extensive grazing and age stratum 7 - 12 months were identified as potential fasciolosis risk factors with the latter being significantly (p<0.05) associated with the disease. On the contrary, home watering, training on livestock husbandry practices and deworming were significant (p< 0.05) protective factors of fasciolosis. Improved husbandry practices assisted by the selective anthelmintic treatments targeting the young animals were identified as feasible fasciolosis control options for Taveta division. In conclusion, the results of the study have clearly shown that fasciolosis is widespread in Taveta Division making it necessary for further longitudinal studies on the disease for establishment of an effective control programme. 

Key words: Epidemiology, prevalence, risk factors, ruminants

Introduction

Fasciolosis is caused by 2 hermaphroditic trematodes, Fasciola gigantica and F. hepatica. Fasciolosis affects most ungulate herbivores although it also occurs in rabbits (Hansen and Perry 1994, Behm and Sangster 1999, Keyyu et al 2005, Pfukenyi et al 2006). The disease has also been reported to affect humans (Mas-Coma et al 2005). Fasciola hepatica whose intermediate host is Galba truncatula occurs in the mild cold climates typical of temperate climates (Mas-Coma and Bargues 1997). On the other hand, F. gigantica is an important parasite for the tropics and occurs throughout the western, sub-Saharan and eastern Africa (Wamae et al 1998, Keyyu et al 2005). The preferred intermediate host of F. gigantica is the lymnaeid snail; Radix natalensisis. Other intermediate hosts associated with F. gigantica in eastern and southern Africa include Galba truncatula and Pseudosuccionea columella (Brown 1994). 

Fasciolosis causes high mortalities especially in small ruminants and calves (Hansen and Perry 1994, Maingi et al 1997, Wamae et al 1998). In sheep, acquired immunity against Fasciola species is poorly developed leading to severe pathology upon infection (Mas-Coma and Bargues 1997) as opposed to cattle in which a strong acquired immunity develops leading to the elimination of most flukes or leading to the development of chronic fasciolosis (Spithill et al 1999). Other than the herd-level losses, fasciolosis also results in losses associated with liver condemnation in slaughtered animals (Kithuka et al 2002, Mungube et al 2006). Other losses associated with fasciolosis include reduced weight gains, poor feed utilization and poor quality of meat and milk products. Despite the considerable economic losses associated with these indirect losses, it is difficult to quantify them. It is only recently that an attempt to estimating the indirect losses was done in one study on fasciolosis in Ethiopia (Berhe et al 2009).  

Fasciolosis control is through elimination of the intermediate host, control of the parasite itself, adoption of good grazing practices (avoiding marshy pastures), regular and rational use of anthelmintics or a combination of all these strategies (Hansen and Perry 1994, Urquart et al 1996). However, anthelmintics are the most preferred due to the private nature (the ease, individual, non-concerted use) of such treatments. However, the development of resistance against the commonly used anthelmintics particularly in the intensive livestock production systems (Boray 1994, Wanyangu et al 1996, Wairuiru et al 1998) is a serious threat that is likely to render majority of the commonly used anthelmintics ineffective in the control of fasciolosis. 

In Kenya, past research on fasciolosis has been concentrated in the intensive livestock production systems of central Kenya highlands, the Rift Valley, Western and sub-humid coastal lowlands (Wamae et al 1998, Wairuru et al 1994, Maingi et al 1997, Muraguri 2000, Kanyari et al 2009). So far, information on fasciolosis in extensively grazed systems is still scanty. Anecdotal evidence indicates that fasciolosis has been reported to occur in Taveta division of Taita Taveta district (MoLD 2009, Mungube et al 2006). It hence justified the need to establish the epidemiology of fasciolosis in this area in order to formulate appropriate control strategies for this disease. An active disease search in live animals and identification of the potential fasciolosis risk factors was undertaken in Taveta division the results of which are described in this paper. 

Materials and Methods

Study area  

The study was undertaken in Taveta division located in the south-east of Kenya on longitudes 37° and 39° E and latitudes 2° and 4° S, respectively. Taveta borders Tanzania to the south, Tsavo national park to the east, and Mwatate division to the north-east. Much of the division lies in agro-ecological zone 4-6 where livestock is the main source of livelihood except where irrigation crop agriculture can be practised. Taveta has two rainy seasons; the long rainy season (March to May) and the short rainy season (October to November) with an annual precipitation amounting approximately 500mm (MoLD 2009). Over 90% of the inhabitants of this division are concentrated in the urban and peri-urban areas of Taveta. In these areas, land sizes average 0.125 acres (MoLD 2009). The rest of the population is in Challa/Njukini area, Lake Jipe area (squatting on Kenya Wildlife Service land), Kiwalwa and Kitogoto.  

Production system 

Mixed crop-livestock production system is practiced in Taveta. Livestock are managed under the intensive and extensive grazing system. Due to the poorly distributed rainfall both in amount and time, flood/furrow irrigation is heavily relied upon in the cultivation of horticultural crops particularly tomatoes, onions, green pepper and bananas. The population in the Lake Jipe settlement in addition to raising livestock also derive a livelihood through fishing on the nearby Lake Jipe.  

The East African zebu and borans and their crosses are kept for milk, meat, manure and socio-economic purposes. The small East Africa goats (SEAG), Galla and few crosses with the exotic breeds like Toggenburg as well as the local Taita sheep, Somali (Black headed Persian) and the Red Masai sheep are reared in Taveta Division. Local scavenging poultry including chicken, ducks and turkeys (mainly in the urban settlement of Bura Ndogo) and a noticeable presence of emerging poultry species including guinea fowls are also present.  

Sampling of settlements and study herds 

Multistage random sampling was used in the selection of settlement areas. Out of the 8 human settlement areas in Taveta, 5 including Kitogoto, Kiwalwa, Bura Ndogo, Challa/Njukini and Lake Jipe area were purposively selected on the advice of the Divisional Veterinary/Livestock office as the main livestock catchment areas.  

A total of 42 herds were selected and used during the study. Bura Ndogo, Challa, Lake Jipe, Kiwalwa and Kitogoto contributed 10, 14, 4, 10 and 3 herds, respectively. Additionally, Gicheha herd specialized in small ruminants was added.  

Study design 

This was a cross-sectional study undertaken in March 2009 which involved appraising the ruminant husbandry practices and screening animals for Fasciola spp. eggs. 

Selection of study animals 

In 5 settlement areas of Bura Ndogo, Kiwalwa, Challa, Kitogoto and Lake Jipe, simple random sampling was used to select study animals. This was done using an estimated fasciolosis prevalence of 25% (Mungube et al 2006) and a desired accuracy level of 5% at 95% confidence level. Following Dohoo et al (2003), the formula below determined the required sample size:

    
Where n = sample size

Z_a  = Z_0.05 = 1.96 (The value of Z_a  required for confidence=95%)

L = the precision of the estimate (allowable error or margin of error) equal to ½ the normal approximation of sample size for the binomial distribution confidence interval. L₂ = 0.0025 or

1/400, p = 25%, the priori fasciolosis prevalence estimate.

Applying this formula, a total of 288 animals would have constituted the optimal estimated sample size. However, in order to improve the precision of the fasciolosis prevalence estimates and to get reliable results, 323 animals were instead selected from the 5 settlements. In addition, 15 animals from Gicheha a privately managed herd were sampled and added to the 323 animals.  

Questionnaire survey 

A standard questionnaire administered to herd owners captured data on grazing, watering, training on livestock husbandry practices and helminth control practices from the selected herds. This was conducted simultaneously with faecal sampling. 

Faecal sample collection and analysis 

Faecal samples were collected per rectum using an arm long sleeve that was later turned inside out and labelled with area, age( estimated by dentition) and categorized as 0 and 6 months, 7 and 12 months and above 12 months,  species, date, sex, herd identity and sample number before storing them in an ice packed cool box awaiting examination. Sedimentation, a qualitative method (Kaufmann 1996) was used to examine the faecal samples for Fasciola species eggs. Briefly, about 5 g of faeces was weighed on a weighing scale and placed into a Petri-dish before adding some water. Using 2 wooden spatulas, the samples were thoroughly homogenized before pouring the mixture through a tea sieve into a 250 ml beaker. The inside of the sieve was then flushed with a hard jet of tap water to force through the adhering fine faecal particles. The beaker was filled three-quarters full with tap water and left standing undisturbed for about 3-5 minutes to allow sediments to settle before decanting. The beaker was refilled with tap water and the above procedure repeated until the overlap was clear. The resultant sediment was transferred into a clean Petri-dish and examined using a compound microscope (magnification 32 diameters) after addition of a few drops of methylene blue. If present, Fasciola species eggs appeared yellow against a bluish background.  

Paramphistomum species eggs were also noted whenever they occurred by differentiating them from those of Fasciola species through their large size, clear colour and operculate nature.  

Data analysis 

Data on husbandry practices were summarized as percentages. Fasciolosis prevalence was calculated as the number of positive faecal samples over the total number of faecal samples examined at settlement, animal species and age-stratum levels. Chi (c²) square tested for differences in fasciolosis prevalence and also for associations with the potential risk factors. The magnitude of association with the risk factors was established through a multivariate binary logistic regression model of the form:  

Fascioslosis odds ratio (In p/1-p) = b_o + b (production system) + b (sex) + b (age) + b (home watering) + b (deworming) + b (husbandry training) as is described under analysis of binary data in Dohoo et al (2003).  

b_o = intercept and b logistic regression exponentiated coefficients (odds ratios) of the variables under question. Odds ratios (ORs), p-values and 95% confidence intervals of the entered risk factors against the outcome of interest (fasciolosis) were reported. These factors were selected from others after a univariate analysis showed they had odds ratios of greater than 1. Paramphistomum species prevalence was estimated as was done for fasciolosis. Data were analyzed in SPSS version 18. 

Results

Livestock husbandry practices  

Of the 42 herds sampled and studied, 66.7% (28/42) practiced mixed crop-livestock production system while pure livestock production system was practiced in 33.3% (14/42) of the herds. Pure livestock production systems were practiced in two settlements; Bura Ndogo 23.8% (10/42) and in Lake Jipe area 9.5% (4/42). Under the pure livestock system, animals in Bura Ndogo were reared under the cut and carry zero grazing system because of the small land size while those in Lake Jipe settlement area were reared under the extensive grazing system. In the mixed crop-livestock systems, only extensive grazing was practised. In the mixed crop-livestock farming, the greater majority (over 90%) of the respondents devoted quality time tending their crops instead preferring to engage herdsmen to look after their livestock. A group of herd owners collectively engaged a common herdsman as a cost-cutting measure. 

Deworming was practised in 57.1% (24/42) of the herds. This targeted weak and sick looking animals only. Only 23.8% (10/42) respondents reported receiving training on proper livestock husbandry practices. In Bura Ndogo where zero-grazing was predominantly practised, all herd owners watered their animals at home as opposed to the other settlements where extensive grazing was practised.   

Fasciolosis prevalence 

Overall fasciolosis prevalence in cattle, goats and sheep for the division was 25.9%, 23.4% and 33.3%, respectively (Table 1). At settlement area level, fasciolosis prevalence was quite varied for each of the ruminant species as is shown in Table 1. Jipe settlement area had the highest (32.1%) fasciolosis prevalence while Bura Ndogo, a more urban area had the least (11.1%) prevalence.  

Disease pressure was positively correlated with grazing system as it was higher in villages where extensive grazing and watering in rivers was practised and lower in zero-grazed herds that were watered at home. Among the animal species, fasciolosis prevalence was highest in sheep and lowest in goats. The age stratum 7 to 12 months had the highest prevalence (Table 2). Inter-species variations in the prevalence based on the age of the study animals were evidently clear. The lowest fasciolosis prevalence in cattle occurred in those aged above 12 months and within the age stratum 0 to 6 months for sheep and in goats.  

Table 3 summarises the potential risk factors for fasciolosis in ruminants in Taveta division. Extensive grazing and age stratum increased fasciolosis occurrence in study animals. However, only age stratum 7 to 12 months was positively associated (OR = 2.34, p=0.01) with disease. On the other hand, home watering with OR=0.03, training on livestock husbandry practices with OR=0.19 and deworming with OR=0.02 had a tendency to reduce (protective factors) risk of occurrence of fasciolosis. 

Other trematode species  

In the study area, Paramphistomum species was also detected with a prevalence of 10.9% (37/338). Despite this, there was a very weak correlation (R² = -0.52; p = 32) between Fasciola species and Paramphistomum species suggesting that the two trematodes rarely occurred together in the same host.  

Prevalence of Paramphistomum spp varied from village to village. Kiwalwa (21.9%) and Bura Ndogo (21.3%) were the most affected villages followed by Kitogoto (10%) and Challa (2.9%). No paramphistome eggs were detected in animals from Gicheha and Lake Jipe area. Prevalence by animal species was 12.2% (24/197) in cattle, 9.9% (11/111) in goats and 6.7% (2/30) in sheep.  

Discussion

The results of this survey clearly show that fasciolosis is endemic in Taveta division. This corroborated the findings of abattoir fasciolosis prevalence survey in the same division (Mungube et al 2006). Fasciolosis prevalence by this study shows that pressure of infection varied across the studied settlements although Lake Jipe area, Challa, Kiwalwa and Gicheha were the most affected. In these settlements, there were vast marshy areas in the community pasture fields where livestock are usually grazed. This increased the risk of animals acquiring new fasciolosis infections in these areas compared to areas with less or no marshy areas in the grazing fields.  

Fasciolosis prevalence of 25.9% in cattle reported by this study approximated the 26% estimated from the abattoir survey earlier conducted in the same division (Mungube et al 2006). Despite the near agreement between the coprological and abattoir fasciolosis prevalence results, it ought to be noted that coprological methods have lower sensitivity but correspondingly higher specificity making them superior over other test systems (Rapsch et al 2006). In addition, coprological screening is labour intensive and is prone to errors including the possibility to misdiagnose eggs of other trematode species as those for Fasciola species.

In comparison, the apparent fasciolosis prevalence of 25.9% in cattle reported by this study was lower than the 34% established in Central Kenya (Waruiru et al 2000). The difference is because exotic cattle breeds are more susceptible to fasciolosis than the indigenous cattle breeds (Castelino and Preston 1979) used in this study. Although, our data did not consider seasonal influences on fasciolosis infection pressure, our results seemed to agree with those from studies conducted in some parts of Africa (Keyyu et al 2005, Pfukenyi et al 2006). 

On the other hand, abattoir survey fasciolosis prevalence that was conducted prior to this study was relatively lower in sheep (5.2%) and in goats (6.6%) as compared to the coprological fasciolosis prevalence in sheep of 33.3% and of 23.4% in goats established by this study. There was hence low agreement between the coprological method and abattoir survey method in sheep and goats. Coprological fasciolosis prevalence estimates were higher than the abattoir survey ones in these two species possibly because fasciolosis in sheep and goats causes an acute disease leading to high mortality among infected animals particularly if they are left untreated (Spithill et al 1999). Due to this peculiar pathology, it is also likely that the immature flukes which extensively migrate via many organs may be missed on meat inspection if scrutiny is restricted to the liver leading to under-reporting. A comparison between sheep and goats showed that sheep were the most affected compared to goats since they graze very close to the ground and were more prone to picking up infective stages of the parasite than goats that browse on shrubs. The same observation was made by Kanyari et al (2009).  

Small ruminant fasciolosis prevalence estimates by this study in sheep (33.3%) and 23.4% in goats) were lower than the 37% in sheep and 36% in goats reported in Nyanza province of Kenya (Kanyari et al 2009). The prevalence in sheep was however lower than the 56.3% reported in Ethiopian highlands (Asrat et al 2005). Maingi et al (1997) observed that in the central highlands of Kenya, sheep mortalities attributed to fasciolosis were as high as 50% on some farms. Although in the present study we never undertook to quantify mortality trends attributed to fasciolosis in sheep, we suspect that fasciolosis kills a lot of sheep in this division, since our results showed that sheep were most affected of the 3 ruminants with the age stratum reporting 66.7% prevalence.  

Logistic regression results showed that home watering, training farmers on livestock husbandry practices and deworming were protective factors of fasciolosis. These three variables were associated with reduced fasciolosis infections in animals. On the other hand, extensive grazing and age stratum 7 months and 12 months were associated with increased fasciolosis infection in animals. They were hence considered as risk factors of fasciolosis. Extensive grazing significantly (p<0.05) increased fasciolosis in livestock. This was due to the continued exposure of livestock to contaminated pastures which in turn increased the risk of acquiring new infections. Since acquired immunity is crucial in influencing the severity of fasciolosis (Mas-Coma and Bargues 1997, Spithill et al 1999), young animals with weak and less developed immunity were more likely to be affected by fasciolosis than older animals in which acquired immunity was well developed. This was illustrated through the outcome of the logistic regression that indicated that animals aged 7 to 12 months had the highest fasciolosis prevalence as compared to those aged above 12 months. This seemed to suggest that sheep above 1 year were likely to better manage fasciolosis as compared to those less than 1 year of age. It ought to be acknowledged that although certain factors like season, herd contacts, economic well being and access to animal health care information among others would have been important during model building, an in depth analysis of each of this was not done as this data was not collected. The interactive and or confounding effects could hence not be assessed in our analysis. 

From this study results, fasciolosis in Taveta can feasibly be controlled through improved husbandry practices particularly through intensification of livestock production systems hence lessening the exposure of animals to Fasciola species in contaminated pasture fields. In addition, selective anthelmintic treatment particularly targeted at young animals and those with clinical disease would be helpful in controlling fasciolosis while avoiding or delaying resistance development (Boray 1994). Although drainage and fencing are effective methods (Urquhart et al 1996) of controlling fasciolosis, they are nonetheless labour intensive and expensive. They also would better be utilized in areas where land ownership is in private hands as opposed to Taveta where land tenure system is still predominantly communal. 

Conclusions and recommendations

• The results of the study suggest that fasciolosis is endemic in Taveta division. Sheep are the most affected animals
  
  
• Livestock owners who have received training on improved husbandry practices had less fasciolosis in their livestock than those who have not been trained on the same
  
  
• Animals aged 7-12 months were the most affected with fasciolosis
  
  
• Deworming helped protect livestock against fasciolosis
  
  
• Further longitudinal studies on this disease with special emphasis on risk factors and mortality trends for recommending an effective control programme.

Acknowledgements

We acknowledge the Kenya Agricultural Productivity Project (KAPP) through the World Bank (IDA) and Government of Kenya for funding this work. Appreciation also goes to the Director Kenya Agricultural Research Institute (KARI) and Centre Director KARI Katumani Research Centre for provision of facilities and for permitting publication of this paper

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Received 5 May 2011; Accepted 6 November 2011; Published 2 April 2012

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