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Research in Veterinary Science 84 (2008) 185193 www.elsevier.com/locate/rvsc

Feeding practices and eects of gastrointestinal parasite infections on live weight gain of small ruminants in smallholder mixed farms in Kenya
A. Odoi
a

a,*

, J.M. Gathuma b, C.K. Gachuiri c, A. Omore

Department of Comparative Medicine, College of Veterinary Medicine, University of Tennessee, 2407 River Drive, Knoxville, TN, United States b Department of Public Health, University of Nairobi, P.O. Box 29053, Nairobi, Kenya c Department of Animal Production, University of Nairobi, P.O. Box 29053, Nairobi, Kenya d International Livestock Research Institute, P.O. Box 30709, Nairobi, Kenya Accepted 26 April 2007

Abstract The objective of this study was to quantify the eects of gastrointestinal nematodosis on live weight gain (LWG) of sheep and goats kept in smallholder farms in Kenya. A total of 307 sheep and goats from smallholder farms were sampled using a 2-stage cluster and systematic random approach. Sampled farms were visited once a month for nine months during which a health and production survey questionnaire was administered, animals weighed and fecal samples taken for fecal egg count. Descriptive statistics and a generalized linear mixed model were performed in SAS. The mean LWG of suckling kids and lambs was low (mean = 46 g/day). High fecal egg count and lack of feed supplementation were identied as the main factors limiting growth. Improved helminth control and nutrition are required to optimize production. 2007 Elsevier Ltd. All rights reserved.
Keywords: Helminths; Nematodosis; Sheep; Goats; Weight gain; Smallholder

1. Introduction With the rapid increase in human population and urbanisation combined with modest increase in incomes in developing countries, the demand for meat and other animal products continues to grow. The unprecedented growth in demand for livestock products has recently acquired the label of the livestock revolution (Delgado et al., 1999, 2001; Mwangi and Omore, 2004). It is therefore becoming increasingly important to optimize agricultural production through improved management practices and the control of production limiting diseases such as helminth infections. The high potential areas of Kenya, of which the central highlands are part, are farmed predominantly by smallholders,
*

Corresponding author. E-mail address: aodoi@utk.edu (A. Odoi).

who are a diverse and growing sector of agricultural community (Sloane, 1986; McDermott et al., 1999; Omore et al., 1999; Muraguri et al., 2004; Wabacha et al., 2004). Gastrointestinal nematodosis is one of the major constraints to production of small ruminants under production systems heavily dependant on pasture grazing (Uriarte and Valderrabano, 1990). Clinical and sub-clinical gastro-intestinal infection, especially that caused by nematodes, is a major health and production constraint in small ruminants and accounts for large economic losses (Fabiyi, 1987; Radostitis et al., 1994; Gatongi et al., 1997). Production losses result from reduction of weight gains, milk yield, birth weights, carcass quality and reduced fertility of female animals (Gatongi et al., 1997). Losses due to haemonchosis alone may amount to approximately US $31 million annually in Kenya (Upton and Gathuma, 1992). In addition, the injudicious use of anthelmintics without due regard to

0034-5288/$ - see front matter 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.rvsc.2007.04.013

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the epidemiological characteristics of the nematodes is a major cause of economic loss (Wanyangu et al., 1996; Maingi et al., 1997). Currently, there is lack of information on small ruminant production from smallholder mixed farming systems in Kenya. Whereas some information on health and productivity of sheep and goats in the range lands has been gathered (ILCA, 1979; Carles, 1980; Carles, 1986; Wilson, 1986), there are very few reports of any quantitative research that have investigated the specic health and production constraints of these animals on Kenyan smallholder mixed farms in the highland areas of the country. Nearly all the information available on the production of small ruminants is from studies conducted in pastoral arid and semi-arid areas, large scale commercial production systems and records from institutional farms and research stations (Carles, 1980, 1986; Coppock et al., 1987; Galaty, 1992; Gatongi et al., 1997; Nganga et al., 2004). Therefore, information on small ruminant production that would be used to help plan and prioritise livestock health interventions, research and give guidance in policy decisions in the highlands is lacking. In the central highlands of Kenya, in particular, no work has been done to assess the health and production levels of sheep and goats in smallholder farms, yet these have a good potential in this area. Moreover, little is known about the interaction of disease with other production factors like husbandry and nutrition because very few farm level studies have been carried out in the smallholder farms in the highlands. Therefore there is need to assess these interactions in the smallholder system in the highland areas of Kenya to inform animal health planning and intervention strategies. The objective of this study was to investigate the impact of gastrointestinal nematode infections on live weight gain of sheep and goats kept under smallholder mixed farming systems in the central highlands of Kenya. 2. Materials and Methods 2.1. Study area The study was conducted in agro-ecological zones (AEZs) 1 and 3 (Jaetzold and Schmidt, 1982) in the central highlands of Kenya. The humid AEZ 1 that receives an average rainfall of 11002700 mm/annum is believed to be a higher agricultural potential zone than the semi-humid AEZ 3 that receives 8001400 mm of rainfall annually. The long rainy season runs from mid-March to the end of May and is followed by a relatively cool and dry spell which gives way to a hot and dry season from August to September. The short rains come in November to December. There is usually little or no rainfall from late December or early January to early March; this dry season is the hottest part of the year. 2.2. Sampling The sampling frame for this study was derived from a dairy characterisation survey (KARI/MOALDM/ILRI,

1996). The above survey sampled households (smallholder mixed farms) from each of the 24 sub-locations in the study area. Survey maps of each of the 24 sub-locations were created in a Geographical Information System (GIS) using ArcInfo GIS software. The survey enumerators, who had previously been trained in the use of the survey instrument, visited their assigned sub-locations, and marked on the sub-location maps the main landmarks. A landmark was dened as any permanent feature such as a trading centre, a school, a church, or a factory (KARI/MOALDM/ILRI, 1996). Two pairs of landmarks were then selected at random for each sub-location, and line transects were drawn joining each pair. Sampling was thereafter done following as closely as possible the marked transects. Every fth household on the left and on the right was included in the survey (KARI/MOALDM/ILRI, 1996). The study area had approximately 30 000 households and the dairy characterisation study sampled a total of 365 of these households. A random sub-sample of the smallholder farms with sheep and/or goats in agro-ecological zones (AEZs) 1 and 3 from the above study was taken for inclusion in the current study. Smallholder farms were dened as those with less than 20 small ruminants. In order to include at least 30% of the sub-locations in the study area, a random sample of nine sub-locations was taken; 5 from AEZ 1 and 4 from AEZ 3. Sampling of sub-locations was necessary to be able to identify the local administrative bodies to be contacted for permission to conduct the study. Thirty three farms with sheep and/or goats were then randomly selected from each AEZ resulting in a total of 66 farms recruited in the study. The number of farms sampled per AEZ was decided upon based on two criteria: (a) logistical feasibility this number would make it logistically possible to visit each farm every month for 9 months. We note that access to some of the farms was dicult during the wet months due to poor road conditions. (b) Statistical power the sample size was deemed large enough to provide meaningful statistical comparisons of the two AEZs. All the animals in the sampled farms (households) were included in the study. The breeds of sheep and goats kept in this area are the East African Maasai sheep and the Small East African goats, respectively. Due to the lack of diversity of small ruminant breeds in the study area, within species breed differences is not expected to be a factor in either mature weight or live weight gains. Sampled farms (households) were visited monthly for 9 months. For the purpose of this study the rst month was used to provide baseline data on weight of the animals upon which weight gain calculations were based. Therefore, results for only 8 months, with data on weight gains, are presented in the results section. 2.3. Data collection Farms were visited monthly for 9 months starting from December 1996 to August 1997. Information gathered during December 1996 visit was used to provide baseline data

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upon which weight gain calculation for January 1997 could be based and are therefore not presented subsequently. During each visit animals were weighed and fecal samples collected per rectum from each animal. The samples were put in plastic fecal bags and transported in a cool box to the laboratory where they were stored at 4 C for periods not exceeding 48 h prior to processing for parasite egg count. Fecal egg counts analysis were performed using the modied McMaster method (MAFF, 1986) using sodium chloride. General farm data including farmer age and sex, years of farming experience and farm size were collected using a questionnaire during the rst visit. In addition, data on basic farm management practices were also obtained during the rst visit. The latter included grazing practices, watering practices, whether or not farmer experienced feed shortage, provision of supplementary feeds, whether or not the animals were grazed o-farm, and anthelmintic use (Table 1). For more detailed information on the data collected using the questionnaire, the complete questionnaire used in the study is available from the corresponding author upon request. We note that most of the farmers did not keep written records. Therefore, to minimize recall bias most of the critical health (fecal egg count) and production data (live weight gain) were collected prospectively during the 8 month follow-up period of the study.

Farmers were instructed to report suspected cases of clinical disease or death to the local veterinary ocers who were requested to ll a specic form containing details of diagnosis and treatment administered. To encourage participation, the farmers were reimbursed for the treatment costs incurred during the study period. Meteorological data, including monthly rainfall totals, were obtained from meteorological stations closest to each of the sampled farms. 2.4. Data handling and statistical analysis The questionnaire and laboratory data were coded into appropriate variables and entered into the database software application, DbaseIV (DbaseIV, Ashton-Tate, California) and statistical analyses done in statistical analysis system (SAS) (PC-SAS, SAS Institute Inc., Cary, North Carolina). Monthly mean weight gains were displayed graphically using Microsoft Excel (Version 2003, 1985 2003, Microsoft Corporation) software. Monthly rainfall totals were superimposed on the above graphs to enable comparisons of the rainfall patterns and weight gain. Summary statistics of farm-, area-, and animal-level variables were computed. Mean live weight gains across levels of categorical variables were computed and presented in a table. Most of the categorical variables of interest for assessment of potential associations with live weight gains were binary. The only categorical variable that was not binary (i.e., grazing systems: tethered, zero-grazing, semi-zero grazing and free-range grazing) was re-coded into a binary variable: zero-grazing (zero-grazing and semi zero-grazing) and none zero-grazing (tethered and free-range). There were also a few continuous variables included in the study. Their crude summary statistics were computed and potential associations with live weight gains assessed using the generalized linear mixed model (GLMM) described below. Variance components analysis was performed to deconstruct the distribution of variance components in weight gains among the variables of interest. Fecal egg count (FEC) was analysed as a continuous variable. The main focus of data analysis was to assess and quantify the impact of FEC on live weight gain, at the animal level, while controlling for other known animal-, farmand area-level confounding variables. As well, it was important to adjust for within-farm correlation (clustering) and the repeated measurements taken during the course of the study. Thus, a GLMM was t to the data using a forwards selection procedure (p < 0.1 for entry and retention) with live weight gain as the outcome variable and FEC as the main explanatory variable. Farms were modelled as random eects and monthly animal measurements within farms were modelled as the repeated eects using rst order autoregressive [AR(1)] covariance structure. Confounders were assessed based on p-values and their impact on the parameter estimate of FEC. Any variable with p-value of at least 0.1 was retained in the model; however, a p-value of 0.05 was used for assessment in the nal model.

Table 1 List of variables investigated in the generalized linear mixed model for the association between live weight gain and fecal egg count of small ruminants in smallholder farms in Kenya, JanuaryAugust 1997 Variable Species Animal age Animal sex Fecal egg count Birth type Body condition Farmer age Farmer sex Years of farming experience Grazing system O farm grazing Feed shortage Purchase of feed Feed supplementation Water source Variable categories Goats versus sheep Continuous variable Male versus female Continuous variable Single versus multiple Good versus poor Continuous variable Male versus female Continuous variable Zero-grazing versus free range/tethered Yes versus no Yes versus no Yes versus no Yes versus no On-farm well; on-farm piped water; o-farm Yes versus no Good versus poor Continuous variable 1 versus 3 Wet versus dry Level (hierarchy) Variable was measured Animal Animal Animal Animal Animal Animal Farm Farm Farm Farm Farm Farm Farm Farm Farm

Anthelmintic use Hygiene Land size Agro-ecological zone Season

Farm Farm Farm Area

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A. Odoi et al. / Research in Veterinary Science 84 (2008) 185193 Table 2 Analysis of weight gains, by month, of small ruminants in smallholder mixed farms in central highlands of Kenya Montha Weight gains per day (g) Mwgb January February March April May June July August 64.80 77.00 3.41 52.37 27.95 44.63 29.48 28.26 SEc 5.5 6.5 4.5 3.8 3.0 3.3 3.4 3.9 Range 350850 318890 493222 469167 271185 159272 338258 300733 Median 59.50 68.18 0.00 45.46 28.57 41.67 21.74 33.33

Additionally, any variable that would result in a change of parameter estimate of FEC of at least 20% would be considered a potential confounder and would be included in the model regardless of its p-value. A list of the variables assessed for potential association and/or confounding eect in the GLMM are listed in Table 1. Due to missing data a total of 60 farms, 260 animals and 1530 observations were used in the GLMM. Note that although a smallholder farm in the study referred to a farm with less than 20 small ruminants, the number of animals available per farm (and thus included in the study) ranged from 1 to 19. All possible two-way interactions of variables retained in the nal model were tested for statistical signicance. None of the two way interactions were statistically signicant at 5% signicance level and therefore none of them were retained in the nal model. 3. Results 3.1. Descriptive statistics The mean age and years of farming experience of the farmers were 52.0 and 21.7 years, respectively. The average land size of the smallholder farms in the study was 4.0 acres. The mean live weight gains over the study period were 46.6 g/day (suckling kids and lambs) and 27.9 g/day (weaners). The monthly live weight gains are shown in Table 2. During each month some animals were losing weight, the largest mean weight loss of which was observed in March (493 g/day). April had the lowest mean weight gains (52.37 g/day) while February had the highest (77 g/ day) (Table 2). The live weight gains were on a downward trend from February to April and began to rise in May,

a December 1996 provided baseline data for calculation of January 1997 weight gains and are therefore not included in the table. b Mean weight gains (g/day). c Standard error.

two months after the onset of rains (Fig. 1). Note that although there was no overall signicant eect of AEZ, Fig. 1 has been presented by AEZ to demonstrate the monthly variation in rainfall patterns and weight gains within and between the two zones. There was a signicant (p < 0.0001) month eect on the mean live weight gains. 3.2. Determinants (predictors) of live weight gains A number of area- farm- and animal-level variables were investigated for potential association with live weight gains. The crude summary statistics of the categorical variables in relation to live weight gains are presented in Tables 3a and 3b. These crude summary statistics seem to suggest potential univariate associations between live weight gains and some of the variables such as sex, season, lack of sup-

Fig. 1. Relationship between weight gains of small ruminants in smallholder mixed farm and rainfall received in AEZs 1 and 3 of the central highlands of Kenya.

A. Odoi et al. / Research in Veterinary Science 84 (2008) 185193 Table 3a Area-, season- and farm-level factors investigated for potential association with live weight gain of small ruminants in smallholder mixed farms in Kenya, 1997 Factor Number (%) of farms Number (%) of small ruminants Number of observations Mwga SEb

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Table 3b Animal-level factors investigated for potential association with live weight gain of small ruminants in smallholder mixed farms in Kenya, 1997 Factor Number (%) of small ruminants Number of observations Mwga SEb

Area-level factors Agro-ecological zone 1 32 (52.5) 3 29 (47.5) Farm-level factors Grazing system Zero29 (44.6) grazing Free36 (55.4) range/ tethered O-farm grazing Yes 13 (21.3) No 48 (78.7) Feed availability No feed 29 (43.9) shortage Feed 37 (56.1) shortage Feed supplementation Yes 24 (36.4) No 42 (63.6) Purchase of feed Yes 17 (25.8) No 49 (74.2) Source of water On-farm 26 (39.4) On-farm 30 (45.5) piped water O-farm 10 (15.1) water source Hygiene Good Poor 20 (32.8) 41 (67.2)

Animal-level factors Species Sheep 236 (76.9) Goats 71 (23.1) 23.1 3.2 31.2 3.0 Animal sex Male Female Birth type Single Twins Body condition Good Poor 103 (34.0) 200 (66.0) 258 (93.8) 17 (6.2) 190 (64.6) 104 (35.4)

1318 469 564 1197 1489 110 1104 608

29 2.6 19 4.4 43.3 3.3 19.4 2.9 34 12.6 28 2.3 31 3.0 21 3.1

134 (43.6) 173 (56.4)

881 906

138 (45.0) 169 (55.0)

655 1120

22.9 3.2 30.6 2.4

83 (27.0) 224 (73.0) 120 (39.1) 187 (60.9)

445 1342 736 1051

37.9 5.4 23.6 2.4 28.5 3.5 26.1 2.9

a b

Mean weight gain. Standard error.

204 (66.4) 103 (33.6) 86 (28.0) 221 (72.0) 104 (33.9) 134 (45.0)

1239 548 357 1328 691 760

29.7 2.9 21.9 3.2 29.6 4.9 27.0 2.7 27.4 3.7 28.3 3.6

65 (21.1)

336

23.7 4.5

119 (38.8) 188 (61.2) 282 (91.9) 25 (8.1) 225 (75.8) 72 (24.2)

643 1144 1395 161 1361 426

29 3.1 25 2.9 31 6.3 16 3.0 27.2 2.7 26.5 3.6

Anthelmintic treatment Yes 52 (78.8) No 14 (21.2) Sex of farmer Male 48 (78.7) Female 13 (21.3) Season factors Season Wet Dry
a b

(9.1%), reducing ock size (9.1%), using unusual forages not normally fed to small ruminants (12.2%) or a combination of the above strategies (43.8%) (data not presented in table). Variance component analysis of the dependent variables and live weight gain revealed that 2% and 19% of the variations in weight gains were attributed to farms and time (month), respectively. Fecal egg count, age, lack of feed supplementation, sex and season were all statistically signicant (p < 0.05) in the nal GLMM model (Table 4). Sex (male) and season (wet) had signicant positive associations with live weight gains whereas FEC, age, and lack of supplementation (yes) had signicant negative association with weight gains. Although the parameter estimates in the GLMM seem small, the impact of these risk factors can be quite important. For instance, lets consider the potential impact of FEC by comparing two animals with dierent FEC values. Assuming the two animals (A and B) are of the same age, sex and are under the same management conditions and the only dierence between them is that animal A has a FEC of 100 epg higher than animal B. Based on the nal model
Table 4 Risk factors of live weight gains of the small ruminants kept in smallholder farms in the central highlands of Kenya, 1997 Parameter Estimate 26.43 45.38 0.98 7.87 0.41 13.20 14.45 SEd 7.4 5.01 0.19 6.70 0.18 5.48 6.95 p-Value 0.0007 <0.0001 <0.0001 0.2404 0.0252 0.0161 0.0377

785 1002

51.9 4.2 10.4 2.4

Mean weight gain. Standard error.

Intercept Season (wet versus dry) Age in months (continuous variable) AEZa (1 versus 3) FECb in EPGc (continuous variable) Sex (male versus female) Lack of feed supplementation (yes versus no)
a b c d

plementation, etc. The farmers used several strategies to overcome seasonal shortages in feed availability; using feed stored during periods when there were surplus (12.2%), reducing quantities of feed (13.6%), purchasing feed

Agro-ecological zone. Fecal egg count. Eggs per gram. Standard error.

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presented in Table 4, and keeping all other factors constant, the impact of this dierence in FEC (i.e., 100 epg) on live weight gain is computed as follows: Dierence in weight gain (A versus B) = Model estimate * Dierence in FEC between A and B. Dierence in weight gain (A versus B) = 0.41 g/day per unit dierence in epg * 100 epg. Dierence in weight gain (A versus B) = 41 g/day (on average). This implies that, if the other variables in the model are held constant, the weight gain of animals with 100 epg higher than their contemporaries of the same age, sex and under same conditions of management will be, on average, 41 g lower. This is quite an important eect on production. Controlling for the other variables in the model, small ruminants that did not get supplementary feeding had weight gains which were on average 14.4 g/ day lower than their contemporaries that received supplementation. Males gained, on average, 13.2 g/day more than females. Controlling for the other variables in the model, a small ruminant that was a month older than its contemporary had a lower weight gain of about 1 g/day. Season had the highest eect on live weight gains since the small ruminants gained on average, 45.4 g/day more in wet season than in dry season. There was no signicant (P > 0.05) difference in live weight gains between small ruminants in AEZ 1 and 3. 4. Discussion This study has shown that the two most important factors that impact live weight gain of small ruminants in smallholder production systems of the central highlands of Kenya are FEC (a proxy of nematode parasite burden) and lack of supplementation. Other studies have reported that worm burden of grazing animals is mainly inuenced by the infection rate from pastures which is, in turn, are determined by climatic conditions that favour hatching of eggs as well as development and survival of larvae (Barger, 1999; Vlasso et al., 2001; Nganga et al., 2004). The observed negative association between FEC and live weight gain is in agreement with reports by a number of other studies (Coop et al., 1976; Parkins and Holmes, 1989; Holmes, 1993; Radostitis et al., 1994; Knox and Steel, 1999). Results of the current study indicate that a small ruminant with, for example, a FEC of 100 eggs per gram of feces higher than it contemporary of same age, sex and under the same conditions of management would gain 41 g/day less weight than its contemporary under the same conditions of management. Invariably, this leads to nancial losses to the farmer in the form of extra time needed for the animals to reach maturity and the obvious cost of anthelmintic treatment. Reducing the impact of FEC on live weight gain will require sustainable helminth control practices that combine strategic anthelmintic treat-

ments based on sound epidemiological data with other means of control such as grazing management (Brunsdon, 1980) and exploitation of resistant breeds (Barger, 1989). Use of pasture spelling in helminth control could also be explored since theres evidence of lack of development of infective larvae during the dry season (Nganga et al., 2004). The decreased weight gain among animals with high FEC may be a direct result of reduction of feed intake (Coop and Holmes, 1996; Kyriazakis et al., 1996; Knox and Steel, 1999) and reduced eciency of feed utilization (Dakkak, 1990; Coop and Holmes, 1996). The reduction in voluntary feed intake is, especially, a major contributor to reduced performance of parasitized animals (Sykes and Coop, 1976; Symons and Hennessy, 1981; Sykes et al., 1988; Sykes and Coop, 2001). Additionally, gastrointestinal nematodosis induces protein deciency by increasing the demand for amino acids in the alimentary tract (Yu et al., 2000; Sykes and Coop, 2001). Detailed studies have shown that there is increased endogenous loss of protein into the gastrointestinal tract, partly as a result of leakage of plasma proteins as well as a result of exfoliation of gut epithelial cells and mucoprotein secretion (Poppi et al., 1986). Moreover, the need to repair parasite damaged tissues, maintain blood homeostasis and mount an immune response increases protein utilization in splanchnic tissue by as much as 40% (Yu et al., 2000) and therefore reduces the amount of protein available for growth and hence the resultant decrease in live weight gain (Sykes and Coop, 2001). The mechanism and priorities of utilization of available nutrients change with the stage of development of the animals immune system (Coop and Kyriazakis, 1999; Sykes and Coop, 2001). In young animals, acquisition of immunity has a higher priority than growth (Sykes and Coop, 2001). Both demands can be met if protein supply is adequate and hence the higher demand for proteins at this time (Bown et al., 1991; Brown et al., 1991; Donaldson et al., 1998; Houdijk et al., 2000; Donaldson et al., 2001). However, if the supply is inadequate, as is the case in this study, development of immunity take priority over growth resulting in the observed reduction in live weight gain and sometimes even weight loss. There is evidence that given a choice between low protein and high protein diets, parasitized sheep change their diet selection in favor of a higher protein diet (Kyriazakis et al., 1994). Furthermore, there is also evidence that intestinal nematode infections can impair the apparent absorption of phosphorus (Wilson and Field, 1983; Poppi et al., 1985; Bown et al., 1989) and cobalt (Ferguson et al., 1989; Grunner, 2001). It is reported that an increase in the phosphorus content of the diet results in increased weight gains (Coop and Field, 1983). Moreover, cobalt deciency may be associated with reduced immunity to nematode parasite leading to a vicious cycle (Ferguson et al., 1989; Grunner, 2001). All these factors interact to cause the observed decrease in weight gain. It is evident that improved nutrition would

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increase host resilience and hence minimize the impact of parasitism on live weight gain. Studies have shown that gastrointestinal nematode parasite induced anorexia is reversed and weight gain increased weeks after anthelmintic treatment of infected animals (Coop et al., 1976). Coop et al. (1976) observed signicantly higher weight gains in infected and anthelmintic treated sheep after the 10th week compared to the infected non-treated group. Moreover, after the 10th week the weight gains in anthelmintic treated groups were similar to those of non-infected animals. Another study by Coop and co-workers reported that mean dry matter intake was reduced by 20% in nematode infected sheep (Coop et al., 1984). However, anthelmintic treatment of infected sheep signicantly improved the rate of weight gain with evidence of compensatory increase in growth (Coop et al., 1984). However, in addition to use of anthelmintics to minimize the impact of nematodosis, there is good evidence that selection of nematode resistant lines of sheep could result in reduction of worm burdens of 1020% (Barger, 1989). The use of genetically resistant hosts should therefore reduce the impact of parasites on live weight gain of the hosts. The signicant negative association between lack of feed supplementation and live weight gain is in agreement with observations made by Knox and Steel in grazing studies with urea molasses block (UMB) supplementation (Knox and Steel, 1996). They reported reduction in live weight gains of animals that were not given supplementary feed as compared to their contemporaries that received supplementary feed. Studies of merino lambs fed low quality roughage diets showed that FEC and worm burdens were lower in lambs supplemented with high protein diet than those that were not supplemented (Knox et al., 1994; Knox and Steel, 1999). Moreover, other studies have reported lower FEC (Theodoropoulos et al., 1998; Datta et al., 1999), as well as higher weight gains and antibody responses in parasitized grazing sheep that had previously received higher protein diet compared to their counterparts that did not receive the high protein diet (Datta et al., 1999). Similar studies in goats showed that FECs were lower and eosinophil counts higher in the animals receiving the high protein diet suggesting that resistance was enhanced by protein supplementation (Etter et al., 2000). There is evidence that protein supplementation boosts the immune system of parasitized animals and increases rate of worm expulsion (van Houtert et al., 1995a; van Houtert et al., 1995b). Houtert and co-workers (1995a) observed up to 13-fold increase in mast cells in animals given supplementary protein. Mast cells and their secretory products have been reported to be involved in the development of resistance to gastrointestinal nematodes (Huntley et al., 1987; Rothwell, 1989; Rothwell et al., 1993; Houdijk et al., 2000). The observed rise in mean live weight gains in May (two months after onset of rains) is attributed to the increased availability of lush grazing pastures resulting from the

increased rainfall a couple of months earlier. Most of the small ruminants in the current study depended on pasture grazing throughout the year. However, forage became scarce during the dry season with negative eect on live weight gains. The negative live weight gains observed in March and April are consistent with observations made by other authors (Carles, 1983; World Bank, 1983; Schwartz and Said, 1986; Coppock et al., 1987; Mucuthi et al., 1994; Wandera et al., 1996) who noted that small ruminant production under traditional systems of management depended on natural pasture whose availability is constrained by erratic rainfall. In the current study, it is evident that periods of starvation coincided with periods of low live weight gains, manifesting as slow maturity in a bid to adapt to low plane of nutrition. Similar observations have been reported in other studies (Devendra, 1981; Devendra, 1982). Moreover, another study in Kenya (Allonby, 1974) reported that a fall in feed quality during the dry months is associated with increased parasitism resulting in reduced weight gains. A number of studies have reported that traditional modes of coping with feed shortage have included shifting and establishment of reserve grazing to be used during the most critical periods of the dry season (Grandin et al., 1991; Galaty, 1992). However, other authors have reported that the herbage from reserve grazing areas are often of low quality and quantity and so only young stock and sick animals are allowed on them (Wandera et al., 1996). Although the farmers in the current study practised shifting to some degree, due to land shortage, they could not practice reserve grazing. Most animals in AEZ 1 were kept under zero-grazing because of the reduced land available due to competition with crop agriculture. Although many of the farmers in this AEZ bought fodder for their small ruminants, these were not sucient during the dry season. The lack of signicant association between feed shortage and feed purchase suggests that the farmers who experienced feed shortage did not necessarily buy the feed; instead they would revert to strategies like use of unusual forages and reducing the amount of feed to the small ruminants. On the contrary, most of the farmers in AEZ 3 also used o-farm grazing as a means of coping with feed shortage and would, therefore, revert to free-range grazing during drought. Most of the farmers who gave the small ruminants supplementary feed were from AEZ 1 (66.7%) most probably due to high income level of these farmers resulting from sale of tea that is not grown in the lower potential AEZ 3. 5. Conclusion High FEC, lack of feed supplementation and season are the three factors that were most signicantly associated with live weight gains of sheep and goats in smallholder farming systems in the central highlands of Kenya. Improvement in the control of helminth infections in these animals oers an opportunity to increase productivity.

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A. Odoi et al. / Research in Veterinary Science 84 (2008) 185193 Dakkak, A., 1990. Gastrointestinal strongylosis and malabsorption of nutrients. Ann. Parasitol. Hum. Comp. 65 (Suppl. 1), 7376. Datta, F.U., Nolan, J.V., Rowe, J.B., Gray, G.D., Crook, B.J., 1999. Long-term eects of short-term provision of protein-enriched diets on resistance to nematode infection, and live-weight gain and wool growth in sheep. Int. J. Parasitol. 29, 479488. Delgado, C., Rosegrant, M., Steinfeld, H., Ehui, S., Courbois, C., 1999. Livestock to 2020: The next food revolution. Food, Agriculture, and the Environment Discussion Paper 28. International Food Policy Research Institute (IFPRI), Food Agriculture Organization of the United Nations (FAO), and the International Livestock Research Institute, Washington, D.C., pp. 72. Delgado, C., Rosegrant, M., Meijer, S., 2001. Livestock to 2020: The revolution continues. Paper Presented at the Annual Meetings of the International Agricultural Trade Research Consortium, Auckland, New Zealand, January 1819, 2001. Devendra, C., 1981. Potential of Sheep and goats in less developed countries. J. Animal Sci. 51, 461473. Devendra, C., 1982. Prospects for Increasing Productivity from Sheep and Goats. Animal Production in the Tropics. Praeger Publishers, New York, USA. Donaldson, J., Van Houtert, M.F., Sykes, A.R., 1998. The eect of nutrition on the periparturient status of mature ewes. Animal Sci. 67, 523533. Donaldson, J., Van Houtert, M.F., Sykes, A.R., 2001. Eect of dietary sh meal supplementation on parasite burdens of periparturient sheep. Animal Sci. 72, 149458. Etter, E., Hoste, H., Chartier, C., Pors, I., Koch, C., Broqua, C., Coutineau, H., 2000. The eect of two levels of dietary protein on resistance and resilience of dairy goats experimentally infected with Trichostrongylus colubriformis: comparison between high and low producers. Vet. Res. 31, 247258. Fabiyi, J.P., 1987. Production losses and control of helminths in ruminants of tropical regions. Int. J. Parasitol. 17, 435442. Ferguson, E.G.W., Mitchell, G.B.B., McPherson, A., 1989. Cobalt deciency and Ostertagia circumcincta infection in lambs. Vet. Record 124, 20. Galaty, J.G., 1992. The land is ours: Social and Economic factors in the privatisation, sub-division and sale of Maasai ranches. Nomadic Peoples 30, 2640. Gatongi, P.M., Scott, M.E., Ranjan, S., Gathuma, J.M., Munyua, W.K., Cheruiyot, H., Prichard, R.K., 1997. Eects of three nematode anthelmintic treatment regimes on ock performance of sheep and goats under extensive management in semi-arid Kenya. Vet. Parasitol. 68, 323336. Grandin, B.E., De Leeuw, P.N., De Souza, M., 1991. Labour and Livestock management. In: Bekure, S., De Leeuw, P.N., Grandin, B.E., Neate P.J.H. (Eds.). Maasai Herding: an analysis of the livestock production system of Maasai pastoralists in Eastern Kajiado District, Kenya., ILCA (International Livestock Centre for Africa), Addis Ababa, Ethiopia. pp. 7182. Grunner, T., 2001. Studies of vitamin B12 metabolism in sheep. Ph.D. thesis, Lincoln University, Lincoln. Holmes, P.H., 1993. Interactions between parasites and animal nutrition: the veterinary consequences. In: Proc. of the Nutrition Society, 52. pp. 113120. Houdijk, J.G., Kyriazakis, I., Jackson, F., Huntley, J.F., Coop, R.L., 2000. Can an increased intake of metabolizable protein aect the periparturient relaxation in immunity against Teladorsagia circumcincta in sheep? Vet. Parasitol. 91, 4362. Huntley, J.F., Gibson, S., Brown, D., Smith, W.D., Jackson, F., Miller, H.R., 1987. Systemic release of a mast cell proteinase following nematode infections in sheep. Parasite Immunol. 9, 603614. ILCA, 1979. International Livestock Centre for Africa. Small Ruminant Production in the humid tropics. In: Proc. of International Livestock Centre for African Addis Ababa, Ethiopia. pp. 5795. Jaetzold, R., Schmidt, H., 1982. Farm Management Handbook of Kenya. In, Ministry of Agriculture, Nairobi, Kenya.

Improvement of the performance of small ruminants in central highlands of Kenya will also require attention to feed supplementation. Low cost supplements that supply nitrogen and essential minerals would enhance the ability of small ruminants to minimize the impact of parasitism. Acknowledgements The authors thank the German Academic Exchange Service (DAAD) and the Department for International Development (DFID) for funding this study. The Kenya Agricultural Research Institute (KARI) provided facilities and sta. We also wish to thank farmers who participated in the study for their co-operation. References
Allonby, E.W., 1974. Studies on Haemonchus contortus infections in merino sheep. Ph.D. thesis, University of Glasgow. Barger, I.A., 1989. Genetic resistance of hosts and its inuence on epidemiology. Vet Parasitol 32, 2135. Barger, I.A., 1999. The role of epidemiological knowledge and grazing management for helminth control in small ruminants. Int J Parasitol 29, 4147 (Discussion 4950). Bown, M.D., Poppi, D.P., Sykes, A.R., 1989. The eects of a concurrent infection of Trichostrongylus colubriformis and Ostertagia circumcincta on calcium, phosphorus and magnesium transactions along the digestive tract of lambs. J Comp Pathol 101, 1120. Bown, M.D., Poppi, D.P., Sykes, A.R., 1991. The eects of abomasal infusion protein or energy on the pathphysiology of Trichostronglylus colubriformis infection and body composition in lambs. Aust. J. Animal Res. 42, 253267. Brown, M.D., Poppi, D.P., Sykes, A.R., 1991. The eects of abomasal infusion protein or energy on the pathphysiology of Trichostronglylus colubriformis infection and body composition in lambs. Aust. J. Animal Res. 42, 253267. Brunsdon, R.V., 1980. Principles of helminth control. Vet. Parasitol. 6, 185215. Carles, A.B., 1980. Productivity of the goat herd at Ngurunit. IPAL Technical Report A-2. Carles, A.B., 1983. Sheep production in the Tropics. Oxford University Press, New York, USA. Carles, A.B., 1986. The levels of and constraints to productivity of goats and sheep at Ngurunit in Marsabit District. In: Smallstock and Cattle. Productivity, Nutrition and Disease in Northern Kenya. I. PAL Technical Report. Coop, R.L., Field, A.C., 1983. Eect of phosphorus intake on growth rate, food intake and quality of the skeleton of growing lambs infected with the intestinal nematode Trichostrongylus vitrinus. Res. Vet. Sci. 35, 175181. Coop, R.L., Holmes, P.H., 1996. Nutrition and parasite interaction. Int. J. Parasitol. 26, 951962. Coop, R.L., Kyriazakis, I., 1999. Nutritionparasite interaction. Vet. Parasitol. 84, 187204. Coop, R.L., Sykes, A.R., Angus, K.W., 1976. Subclinical trichostrongylosis in growing lambs produced by continuous larval dosing. The eect on performance and certain plasma constituents. Res. Vet. Sci. 21, 253258. Coop, R.L., Angus, K.W., Hutchison, G., Wright, S., 1984. Eect of anthelmintic treatment on the productivity of lambs infected with the intestinal nematode, Trichostrongylus colubriformis. Res. Vet. Sci. 36, 7175. Coppock, D.L., Ellis, J.E., Swift, D.M., 1987. Seasonal food habits of livestock in South Turkana, Kenya. East African Agric. J. 3, 96207.

A. Odoi et al. / Research in Veterinary Science 84 (2008) 185193 KARI/MOALDM/ILRI, 1996. Kenya Agricultural Research Institute/ Ministry of Agriculture, Livestock Dev. and Marketing/International Livestock Research Centre (KARI/MOALDM/ILRI) Results of a pilot dairy systems characterisation survey in Kiambu District, Kenya. In: Proc. of National Agricultural Research Centre, Kikuyu, Kenya, Nairobi, Kenya. Knox, M., Steel, J., 1996. Nutritional enhancement of parasite control in small ruminant production systems in developing countries of SouthEast Asia and the Pacic. Int. J. Parasitol. 26, 963970. Knox, M.R., Steel, J.W., 1999. The eects of urea supplementation on production and parasitological responses of sheep infected with Haemonchus contortus and Trichostrongylus colubriformis. Vet. Parasitol. 83, 123135. Knox, M.R., Steel, J.W., Leng, R.A., 1994. The eects of urea supplementation on gastrointestinal parasitism in sheep being fed low quality roughage diets. In: Proc. of Australian Society of Parasitology 30th Annual Scientic Meeting, Nelson Bay, NSW. p. 28. Kyriazakis, I., Oldham, J.D., Coop, R.L., Jackson, F., 1994. The eect of subclinical intestinal nematode infection on the diet selection of growing sheep. Br. J. Nutri. 72, 665677. Kyriazakis, I., Anderson, D.H., Oldham, J.D., Coop, R.L., Jackson, F., 1996. Long-term subclinical infection with Trichostrongylus colubriformis: Eects on food intake, diet selection and performance of growing lambs. Vet. Parasitol. 61, 297313. MAFF, 1986. Ministry of Agriculture Fisheries and Food Britain. Manual of Veterinary Parasitological Laboratory Techniques, London, United Kingdom. Maingi, N., Bjorn, H., Thamsborg, S.M., Munyua, W.K., Gathuma, J.M., Dangolla, A., 1997. Worm control practices on sheep farms in Nyandarua District of Kenya. Acta Trop. 68, 19. McDermott, J.J., Randolph, T.F., Staal, S.J., 1999. The economics of optimal health and productivity in smallholder livestock systems in developing countries. Rev. Sci. Technol. 18, 399424. Mucuthi, M.M., Munei, K., Sharma, K.C., 1994. Some socio-economic factors that aect decisions on small ruminant production by smallscale farmers. A case study of West Laikipia. In: proc. of Small Ruminant Research and Development in Africa 1994. pp. 2327. Muraguri, G.R., McLeod, A., Taylor, N., 2004. Estimation of milk production from smallholder dairy cattle in the coastal lowlands of Kenya. Trop. Animal Health Prod. 36, 673684. Mwangi, D.M., Omore, A., 2004. The livestock revolution a view on implications for Africa. In: Owen, E., Smith, T., Steele, M.A., Anderson, S., Duncan, A.J., Herrero, M., Leaver, J.D., Reynolds, C.K., Richards, J.I., Ku-Vera, J.C. (Eds.), Responding to the Livestock Revolution. BSAS Publication No. 33. ISBN: 1-90476151-8. Nottingham University Press, pp. 5165. Available at www.nup.com. Nganga, C.J., Maingi, N., Kanyari, P.W., Munyua, W.K., 2004. Development, survival and availability of gastrointestinal nematodes of sheep on pastures in a semi-arid area of Kajiado District of Kenya. Vet. Res. Commun. 28, 491501. Omore, A.O., McDermott, J.J., Arimi, S.M., Kyule, M.N., 1999. Impact of mastitis control measures on milk production and mastitis indicators in smallholder dairy farms in Kiambu district, Kenya. Trop. Animal Health Prod. 31, 347361. Parkins, J.J., Holmes, P.H., 1989. Eects of gastrointestinal helminth parasites on ruminant nutrition. Nutri. Res. Rev. 2, 227246. Poppi, D.P., MacRae, J.C., Brewer, A.C., Dewey, P.J., Walker, A., 1985. Calcium and phosphorus absorption in lambs exposed to Trichostrongylus colubriformis. J. Comp. Pathol. 95, 453464. Poppi, D.P., MacRae, J.C., Brewer, A., Coop, R.L., 1986. Nitrogen transactions in the digestive tract of lambs exposed to the intestinal parasite, Trichostrongylus colubriformis. Br. J. Nutri. 55, 593602. Radostitis, O.M., Leslie, K.E., Fetrow, J., 1994. Health and production management for sheep. In: Herd Health: Food Animal Production Medicine. W.B. Saunders Company. Rothwell, T.L., 1989. Immune expulsion of parasitic nematodes from the alimentary tract. Int. J. Parasitol. 19, 139168.

193

Rothwell, T.L., Windon, R.G., Horsburgh, B.A., Anderson, B.H., 1993. Relationship between eosinophilia and responsiveness to infection with Trichostrongylus colubriformis in sheep. Int. J. Parasitol. 23, 203211. Schwartz, H.J., Said, A.N., 1986. Sheep and goat Nutrition on natural pastures in Kenya. In: A deniji, K.O., Kategile, J.A. (Eds.), Proc. of a Workshop on improvement of small ruminants in Eastern and Southern Africa OAU/IDRC Nairobi, Kenya. pp. 127133. Sloane, P.H., 1986. Population Supporting Capacity Studies for Kenya: Animal Production study. A Proposed Model for Estimating the Human food Supply produced by animals in Kenya. FAO, INT/ 75P13. Sykes, A.R., Coop, R.L., 1976. Intake and utilization by growing lambs with parasitic damage to the small intestine caused by daily dosing with Trichostronglylus clubriformis larvae. J. Agric. Sci. 86, 507515. Sykes, A.R., Coop, R.L., 2001. Interactions between nutrition and gastrointestinal parasitism in sheep. NZ. Vet. J. 49, 222226. Sykes, A.R., Poppi, D.P., Elliot, D.C., 1988. Eect of concurrent infection with Ostertagia circumscincta and Trichostrongylus colubriformis on the performance of growing lambs consuming fresh herbage. J. Agric. Sci. 110, 531541. Symons, L.E., Hennessy, D.R., 1981. Cholecystokinin and anorexia in sheep infected by the intestinal nematode Trichostrongylus colubriformis. Int. J. Parasitol. 11, 5558. Theodoropoulos, G., Zervas, G., Koutsotolis, K., Nikolaou, E., Kalogiannis, D., Petrakos, G., 1998. The eect of dietary protein levels before turnout on subsequent faecal nematode egg output of grazing sheep in the Joannina region of Greece. Res. Vet. Sci. 65, 269271. Upton, M., Gathuma, J.M., 1992. KARI/ODA Helminthology Project: Consultancy in Economics and Epidemiology. In: Proc. of PAN Livestock Services, Reading, UK. Uriarte, J., Valderrabano, J., 1990. Grazing management strategies for the control of parasitic diseases in intensive sheep production systems. Vet. Parasitol. 37, 243255. van Houtert, M.F., Barger, I.A., Steel, J.W., 1995a. Dietary protein for young grazing sheep: interactions with gastrointestinal parasitism. Vet. Parasitol. 60, 283295. van Houtert, M.F., Barger, I.A., Steel, J.W., Windon, R.G., Emery, D.L., 1995b. Eects of dietary protein intake on responses of young sheep to infection with Trichostrongylus colubriformis. Vet. Parasitol. 56, 163 180. Vlasso, A., Leathwick, D.M., Heath, A.C., 2001. The epidemiology of nematode infections of sheep. NZ. Vet. J. 49, 213221. Wabacha, J.K., Maribei, J.M., Mulei, C.M., Kyule, M.N., Zessin, K.H., Oluoch-Kosura, W., 2004. Health and production measures for smallholder pig production in Kikuyu Division, central Kenya. Prev. Vet. Med. 63, 197210. Wandera, F.P., Audi, P., Sitienei, J.K., Ahuya, C.O., Munene, W.N., Wanyangu, S.W., 1996. Results of a PRA study in Kajiado and Baringo Districts. In: Kenya Agricultural Research Institute (KARI) (1997). Manual of Livestock Production Systems. KARI/ODA Socioeconomics and Epidemiology Project. National Veterinary Research Centre, Kikuyu, Kenya. Wanyangu, S.W., Bain, R.K., Rugutt, M.K., Nginyi, J.M., Mugambi, J.M., 1996. Anthelmintic resistance amongst sheep and goats in Kenya. Prevent. Vet. Med. 25, 285290. Wilson, R.T., 1986. Strategies to increase sheep production in East Africa. FAO 58, Small Ruminant Production in the developing countries. Wilson, W.D., Field, A.C., 1983. Absorption and secretion of calcium and phosphorus in the alimentary tract of lambs infected with daily doses of Trichostrongylus colubriformis or Ostertagia circumcincta larvae. J. Comp. Pathol. 93, 6171. World Bank, 1983. Sheep and goats in Developing countries; their present and potential Role. A World Bank technical paper. pp. 174. Yu, F., Bruce, L.A., Calder, A.G., Milne, E., Coop, R.L., Jackson, F., Horgan, G.W., MacRae, J.C., 2000. Subclinical infection with the nematode Trichostrongylus colubriformis increases gastrointestinal tract leucine metabolism and reduces availability of leucine for other tissues. J. Animal Sci. 78, 380390.

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