A high rate of internal parasite infestation was reported by Waller (1997b) and Kochapakdee et al (2001) for grazing ruminants in the humid tropics especially in the SE Asia region. More often, the negative effect on livestock productivity due to intestinal parasites, especially with Coccidia, Haemonchus and Trychostronglylus, was recognized to be more harmful than other problems (Kochapakdee et al 1991). In most cases the opportunity to use anthelmintics is not very easy when the animals are kept in smallholder free-ranging systems. Lack of access to anthelmintics may lead to low productivity when the flock is infected, as routine treatment may be required. About 30% of the goat farms in Cambodia used anthelmintic to treat the animals whereas more than 50% did not do so, probably because of limitations of capital or knowledge (Goat Project report, TAG 433, 2001).
The problem of anthelmintic resistance is being recognized as a major threat to livestock production. Significant benefits are likely to emerge from research into non-chemotherapeutic approaches to nematode parasite control including host genetic resistance, grazing management, worm vaccines and biological control (Waller 1997a). Among these approaches, the use of plants containing anti-parasitic compounds would appear to an appropriate and easily accepted strategy, especially for smallholder farmers, who in their traditional practices often use herbal medicines.
Condensed tannins (CT) have been shown to have an effect on pathogenic micro-organisms beside inhibiting cellulose digesting microbial enzymes in the ruminant (Barry et al 1986). Forsberg and Cheng (1990) also reported that high levels of condensed tannins could affect enzymatic activity and bacterial growth, which might contribute to the poor digestion of forages containing these compounds. In contrast, it has been shown that a low and medium concentration of CTs could have beneficial effects on the ruminant by enhancing nutrient metabolism especially protein digestion and absorption in the intestines (Barry and McNab 1999). More recently, a very important role of CTs has been found, having both direct and indirect effects on nematode parasites in ruminants (Butter 2001).
Condensed tannins have been found in many kinds of plants and forages used as animal feed. Research to promote the use of cassava as a forage source in the tropics has drawn attention to the important role of the CTs present in cassava leaves (Wanapat 2001). This research has shown the direct effect of cassava leaves in the diet, both in fresh and dried form, in reducing the numbers of parasite egg voided in the faeces of ruminants infected with nematodes (Netpana et al 2001; Seng Sokerya and Rodriguez 2001; Granum et al 2003).
Nematode infection is one of the major causes of wastage and decreased productivity in goats worldwide, particularly under grazing conditions and overstocking of pastures that generally promotes increased parasitism (Kehlbach and Nguyen Quang Suc 1997). It seems that goats are more susceptible to internal parasites than sheep and cattle (Peacock 1996). The nematodes have a very simple and direct life cycle, which does not involve any intermediate host. Adult nematodes live in the gastro-intestinal tract, where they mate. The female worms can produce 10000 eggs daily and these pass out of the goat in the faeces. First stage larvae develop and hatch after about 1 to 2 days and become the second stage larvae (infective larvae) in the next 4 to 6 days. The time taken by the larvae to develop from egg to infective larvae depends on the climatic conditions and species of the parasite. If it is warm and wet, they may become infective larvae after 7 to 10 days, but they will take longer if it is colder. These infective larvae remain encased outside and migrate in to the herbage until it is ingested by grazing animals. The sheath is cast off in the abomasum of the animals and the parasite third stage larvae develop and move to the fourth stage. The fourth stage sooner or later molts to the fifth or adult stage in 17 to 20 days after infection, depending on whether or not it enters a period of arrested development. They can survive about 6 to 8 months inside the animal's body (Sourn Sothoeurn 1995; Georgi and Georgi 1990).
The consequences of gastrointestinal parasitism in ruminants are impaired production and even death. Severe, untreated infection may be fatal and an obvious cause of economic loss. But non-fatal infections, apart from resulting in poor productivity, also cause affected animals to be culled prematurely and thus not be available for use as replacement breeding stock. The slow rate of attaining maturity in ruminants, due to chronic sub-clinical parasitism in combination with malnutrition and poor management, may have more impact than directly mortality (Parklins and Holmes 1989, cited by Bullerdieck 1996). Of all the gastro-intestinal parasites that affect goats, Haemonchus contortus is by far the most important species, which is distributed world-wide, especially in warm areas (Sourn Sothoeurn 1995; Dormey et al 1995). The kids are more susceptible to parasite burdens than the older animals and often die from them.
The effect on goats will depend on the number of parasites and on the nutritional status of the animal. The main symptoms of parasitic infection are weight loss, reduced feed intake, reduced milk production, pale mucus membranes from anemia, diarrhea and sometimes death. Parasite infection will dramatically reduce milk production, which can have a drastic effect on the suckled kids. If the dam is infected, the chances are high that the kids will also become infected. If the kids are already weak from the lack of milk, they will have a poor chance of survival. This combination of factors is one of the main causes of death among kids (Peacock 1996).
When four-month-old lambs were infected by repeated drenching with H. contortus larvae (300 larvae twice per week), they began to show impaired weight gain and a 2.5% reduction in Packed Cell Volume (PCV) during the first six weeks after infection (Shaw et al 1995). Six weeks after a primary infection with T. colubriformis, five month old cross-bred lambs stopped growing. During 20 weeks of the experimental period, infected lambs had a 50% reduced liveweight gain (Kimambo et al. 1988a, 1988b, cited by Bullerdieck 1996). At peak infection, the naturally acquired population of Haemonchus contortus may remove one fifth of the circulating erythrocytes per day from the lamb and may on average remove one tenth of the circulating erythrocyte volume per day which is about 0.05 ml blood lost per day for each worm. So in case of an acute condition where there are 2000 worms and more, then the animal will lose up to 10 ml blood per day (Sourn Sothoeurn 1995). The pathogenic effect of Haemonchus results from the inability of the host to compensate for blood loss. If the blood loss exceeds the host hematopoietic capacity, either because the challenge is over whelming or because the response is handicapped by poor nutrition, defective phenotype, or stress, a progressive anemia leads rapidly to death (Georgi and Georgi 1990).
Drug resistance means the ability of a parasite to survive at what was previously determined to be lethal concentrations of a toxic drug (McGill University, no date). Resistance capacity increases when worms are exposed frequently to the same drug, especially when there is significant pasture contamination and a genetic trait of the worm develops, showing appearance within a population to occur through generations.
In traditional systems of small ruminant production in the tropics, helminth control is hardly practiced due to either the lack of awareness on the part of livestock owners or the relatively high cost and scarcity of modern anthelmintics. However, if control programs are implemented they are usually based only on chemicals and often the treatments are not given at the right time (Tembelyl and Hansen 1996). In most cases the opportunity to use anthelmintics is not very easy when the animals are kept in smallholder free-ranging systems. Lack of access to anthelmintics may lead to low productivity when the flock is infected as routine treatment may be required. However re-infestation can occur 4 to 6 weeks after drenching with anthelmintic (Kochapakdee et al 2001). Anthelmintic resistance is becoming more important in goat husbandry when anthelmintics are applied at high levels with increasing frequency and with inappropriate doses (Pandey et al 2001). In other cases, livestock trading causes migration of the parasite. Because nematode populations show great genetic variation and environments vary widely, the response to anthelmintics may be variable. Worms that are resistant to anthelmintic treatment pass on this resistance to their offspring (Prichard 2001). Now, resistance to the various classes of anthelmintics is widespread in nematodes that parasitize sheep and goats (Conder and Campbell 1995; Mckenna 1995).
Because of the global nature of the anthelminthic resistance problem, the need for alternative methods to control nematode parasites are being studied. Those methods include:
Grazing management systems to reduce infection include: letting animals graze for not more than 4 days on the same pasture and allow one month to free the pasture before animals return (SParC Newsletter 1999). The Rapid Rotational Grazing System (RRGS) minimises parasite infection by breaking the parasite life cycle in the pasture using a system of dividing the available grazing area into 10 paddocks. Deworming of the goats may be required before starting the rotational system (SParC Newsletter 2001). Grazing together more than one species of animals can help to break the parasite life cycle as several parasite species cannot infect two different animal species (Duval 1994). Beside this, avoiding wet areas to decrease risk of liver flook infection is another kind of controlled grazing.
Resistance means the ability of a host to reduce the number of parasites that reproduce or survive. A host with higher resistance is less susceptible. This is one option for overcoming the impact of infectious disease in small ruminants by identifying and using disease-resistant animals or breeds (Baker 1995), as the enhanced resistance to nematode parasite infections is a heritable trait (Zajac 1995). Gray (1995) has described the concepts of resistance and resilience as criteria for selection and breeding, within the environment in which the selection takes place. Breeding strategies involve a two stage selection process. The first stage is a preliminary culling of animals based on their (poor) productivity, followed by faecal egg count (FEC) measurements on those remaining (Woolaston et al 1995).
An important factor in the pathogenesis of GI nematode infection is a reduction of feed intake by the host and increased endogenous protein losses, which result in the net loss of amino acids to the parasitized host. Martin et al (1996) indicate that resilience and resistance to GI nematodes can be enhanced by increasing the metabolizable protein supply to the host animal. The main effect of protein supplementation is to increase the rate of acquisition of immunity and increase resistance to re-infection through an associated enhanced cellular immune response in gastrointestinal mucosa (Coop and Holmes 1996). It has been shown that mineral and non-protein nitrogen supplements can lead to greater feed intake and increase microbial protein production, which in turn increases protein digestion and absorption in the small intestine. This process provides a better capacity to the animal to withstand the parasite, as well as supporting higher growth rate with reduced loss of productivity and mortality (Waller 1999; Knox and Steel 1996). Nutrition can affect the ability of the host to cope with the consequences of parasitism and to contain and eventually to overcome parasitism. It can also affect the parasite population through the intake of anti-parasitic compounds (Coop and Kyriazakis 2001).
The objective of this approach, which is to break the life cycle of the nematodes by the use of nematode-trapping fungi to control worm infections, is based on targeting free-living stages on pasture rather than parasitic stages in the host (SParC Newsletter 2000). Recent advances in the development of practical means of deploying nematophagous fungi as biocontrol agents of nematode parasites for a range of livestock species clearly indicate that this may be the first non-chemical alternative to parasite control (Waller 1996). The nematophagus fungus, Duddindtonia flagrans, was subjected to a number of in vivo investigations to determine its capacity to survive through the intestinal tract. Chlamydospores released from such devices can substantially reduce the number of infective larvae derived from nematode eggs in faeces (Larsen et al 1998) and the number of infective larvae that develop in cultures of faeces collected from sheep infected with the nematode parasite (Waller et al 2001). Feeding D. flagrans and intra-ruminal infusion resulted in reduced faecal egg counts and fewer larvae in the faeces and pasture, and also tended to improve liveweight gains (Knox and Faedo 2001; Faedo et al 1998).
Parasite populations can also be affected through the intake of anti-parasitic compounds using plants instead of drugs as a way of getting around this problem. The plants are usually free of charge and represent a “ready to go” anthelmintic, so it is perfect for the farmers. Others call it ‘traditional’ or ‘ethnoveterinary’ medicine. All these expressions refer to the practices of farmers and herds-folk who treat their stock with plant parts or extracts. Justine Jovellanos found that dried leaves of pineapple (Ananas comosus) or custard apple (Anona squamosa) dramatically reduced egg counts in nematode-infected cattle (SParC 4 2000). Neem leaves (Azadirachta indica) were also found to have an effect in reducing the number of H. contortus in the abomasums of the treated sheep (Brelin 2002). Chenopodium ambrosioides oil was reported to reduce the availability of nematode eggs in an in vitro test and was expected to be useful as a long-term ecological strategy to reduce parasite loads (Ketzis et al 2002).
A limitation affecting the use of tree and shrub foliage as feed for ruminants may be a too-high content of tannins and other anti-nutrients, which limit nutrient utilization. The two main categories of tannins that impact animal nutrition are hydrolyzable tannins (HTs) and condensed tannins (CTs) that are resistant to hydrolytic degradation. HTs are usually present in low amounts in plants.
Tannins are known to have detrimental effects on animal performance by reducing intake and digestibility of forages, which enhance the loss of endogenous proteins and affect overall nitrogen metabolism in the animal (Meissner and Paulsmeier 1995; Silanikove et al 2001; Mcsweeney et al 2001). CTs decrease digestion of organic matter, fiber and protein. As they are not absorbed by the digestive tract, CTs may damage the mucosa of the gastrointestinal tract, decreasing the absorption of nutrients and essential amino acids. The most susceptible amino acids are methionine and lysine. Decreasing the methionine availability could increase the toxicity of cyanogenic glycosides, because methionine is involved in the detoxification of cyanide via methylation to thiocyanate (Cornell University 2001). They bind feed proteins and enzymes to form protein-tannin complexes, which are resistant to both rumen microbial and enzymatic degradation and lower the enzyme activity (Aufrere et al 1995), and interfere the normal process of rumen degradation of microbial attachment to the feed (Frutos et al 2002).
CTs are well known as having a negative effect on nutritive value of feeds (Windham et al 1990), when their concentration exceeds 6% of the DM in plants used as feed. At concentrations of from 75 to 100 g/kg DM, they depressed voluntary feed intake and rumen carbohydrate digestion and depressed rates of body and wool growth in grazing sheep (Barry and McNab 1999). However, these effects vary depending on the content and type of tannin ingested and on the animal's tolerance, characteristics of the digestive tract, feeding behavior, body size, and detoxification mechanisms.
Some animals are able to adapt to tannins using several available mechanisms, such as alkaline gut pH, presence of surfactants to decrease affinity between ingested tannins and protein, presence of peritrophic membranes that absorb tannins and are then excreted in the feces (Cornell University 2001). Many animals that regularly consume tannin-rich feeds appear to develop defensive mechanisms against this compound such as secretion of proline-rich proteins (PRPs) in the saliva, which is considered to be the first line of defence against dietary tannins. Therefore, less protein is required to bind all the tannins, resulting in a quantitative saving of nitrogen (Makkar 2001). There are species differences in the amount of PRPs that different species produce to bind tannins (deer> goat> sheep> cattle). It is suggested that consumption of high-tannin diets stimulates the development of the salivary glands to permit more PRP production. However, some researchers claim that sheep and cattle do not have any PRPs (Cornell University 2001).
The presence of tannins in feed sources for monogastric animal species is generally viewed adversely, though their contribution to red wines is certainly an exception. However, in ruminants, tannins can induce beneficial effects. The main effects on the nutritional metabolism that occur in the digestive tract are: enhancing rumen escape, increasing efficiency of nitrogen recycling to the rumen and increasing microbial growth efficiency. In diets based on tanniniferous forages, nitrogen outflow from the rumen is often greater than nitrogen intake. It has been reported that when moderate doses of tannins are used there would be an increase in protein flow due to the increase of rumen escape of dietary proteins and an increase in microbial protein flow (up to 28% in sheep) according to Cornell University (2001). Fassler and Lascano 1995 noted lower levels (2 to 4%) of tannins could have beneficial effects on ruminant animals, by suppressing bloat and reducing excessive degradation of high quality protein in the rumen. This helps in increasing the amount of rumen undegradable protein, which is finally made available to the host animal for supplying essential amino acids. The study of Barry and McNab (1999) has also indicated the action of CTs in Lotus corniculatus, which in a minimum concentration (5 g/kg DM) help to prevent rumen frothy bloat in cattle. Sheep grazing CT-containing legumes were shown to better tolerate internal parasite infections than sheep grazing non CT-containing forages. Medium concentrations (30 to 40 g/kg DM) increased the absorption of essential amino acids from the small intestine and increased wool growth, milk secretion and reproductive rate in grazing sheep without affecting voluntary feed intake.
Normally CTs of various temperate herbaceous species have the potential to be of benefit to parasitised animals through increasing the supply and absorption of digestible protein which will indirectly improve host resistance and resilience to GI nematodes. CT-containing forages and CT extracts also directly assist in reducing infection by GI nematodes by mechanisms, which do not appear to be mediated through digestible protein supply (Kahn and Diaz-Hernandez 2000). These authors showed that CTs extracted from a number of woody plants were able to reduce in vitro nematode viability., Support for this finding comes from observations of a direct anthelmintic effect of CTs on GI parasites in an experiment with parasitized sheep, which were drenched with a Quebracho CT extract for only seven days (Athanasiadou et al 2000). The effect of dietary quebracho tannin (40 g/kg) on the establishment of parasitic nematodes in the small intestine was conducted in order to determine whether this occurs through direct toxicity against the parasites both in vivo and in vitro studies. It was indicated that dietary quebracho tannin may reduce nematode worm burdens through a toxic effect that requires direct contact between parasite and tannin (Butter et al 2001). However, it is not possible to predict the anti-parasitic properties of plant species simply by their CT content because different plants contain CTs with very different structures and hence different degrees of reactivity against parasites and with animal nutrition (Mueller-Harvey 1999).
Cassava is a highly productive tropical crop that is traditionally cultivated to produce roots for human consumption or industrial extraction of starch. In 1999 Cambodia had 7000 ha for cassava plantations, which yielded the production about 67,500 of roots (FAO 2000). The leaves are a by-product from this operation and can be sun-dried prior to using them as a source of protein and vitamins in pig and poultry diets (Ravindran 1991). Moreover, it could be considered to have a good potential to use as forage because the high level of protein in the leaves (Reed et al 1982). The other approach to cassava cultivation is to manage it as a semi-perennial forage crop with repeated harvesting at 2 to 3 month intervals (Preston et al 2000; San Thy and Preston 2001). In this case, the roots are not harvested but serve as a nutrient reserve to support the forage re-growth. However, according to Wanapat et al (1997), harvesting the cassava leaves after 3 months re-growth would result in higher levels of CTs as well as of protein, and this might limit the use of the cassava foliage.
Cassava leaves generally contain more that 20 % crude protein (Reed et al 1982; Wanapat 1999; Keir et al 1997; Duong Nguyen Khang and Wiktorsson 2001). This is the basis for the development of feeding systems that utilize the aerial part of cassava in different forms such as meal, hay and fresh foliage. The most nutritious part is the leaf, in view of the report of crude protein concentrations in DM of 8.83, 9.63 and 32.6 %, in stem, petiole and leaf, respectively (Seng Sokerya and Preston 2003). Cassava leaves are also good sources of minerals, particularly Ca, Mg, Fe, Mn and Zn and are also rich in ascorbic acid, vitamin A, and contain significant amounts of riboflavin (Ravindran 1991). Cassava leaf protein is low in methionine and tryptophane, but rich in lysine (Eggum 1970; Rogers and Milner 1963, cited by Ravindran 1991). The amino acid content of the leaves varies with different stage of maturity, sampling procedures, analytical methods and ecological conditions. Ravindran and Ravindran (1988) showed that in matured leaves, the amino acid concentrations tend to decrease; lysine and histidine showed the greatest decrease among all the essential amino acids.
The normal range of cyanide content in cassava leaf is from 20 to 80 mg HCN per 100 g fresh leaf weight or from 800 to 3200 mg/kg in dry basis, which is substantially higher than the normal range of HCN reported for fresh cassava roots (Ravindran 1991). Variety and stage of maturity are perhaps the major factors causing variations in the cyanide content in cassava leaf (Chhay Ty and Rodriguez 2001; Chhay Ty et al 2003). HCN toxicity in monogastric animals has been discussed in many reports; however, it does not appear to be a a problem for ruminants as it can be detoxified by the rumen microorganism (Preston 1995). In my research paper (Seng Sokerya et al 2003), it was shown that despite a concentration of HCN in the cassava foliage of 653 mg/kg of DM, there were no symptoms related to depression in nutritive value or toxicity. For goats, it is perhaps more important to concentrate the research on the role of the tannins in cassava, in view of their potential benefits as described in earlier sections of this review.
Reed et al (1982) stated that condensed tannin may be the important factor limiting the use of cassava. The concentrations of tannins in the plant depend on the maturity and vary according to methods of cultivation. The tannin content in cassava has been reported to vary from 30 to 50 g/kg DM (Ravindran 1993), and from 39 and 43 mg/kg in cassava hay and dry cassava leaf (Wanapat 2001). Levels of 32.6 and 40 mg/kg in cassava hay were recorded by Netpana et al (2001) and Granum et al (2003). This range of CT has been reported to be beneficial to ruminants, as it enhances the use of the protein as well as playing an anthelminthic role for the control of nematode parasites (Fassler and Lascano 1995; Barry and McNab 1999; Butter et al 2001). In my research (Seng Sokerya et al 2003), the CT content in fresh cassava leaves was 41.5 mg/kg DM, and was associated with improved growth and a low EPG in the faeces of the goats in each of two experiments.
In Thailand, cassava foliage has been made into “hay” as a means of conservation and to reduce the content of CTs and improve it as a source of bypass protein for dairy cattle (Wanapat et al 1997). Fresh cassava foliage is also a satisfactory protein supplement. However, Ravindran (1991) considered that it should be wilted before feeding and prudently used for good results. No adverse effects on performance were reported even when higher levels of wilted cassava foliage were offered to goats and sheep. The purpose of wilting is to prevent cyanide toxicity and also to reduce the free tannin levels and improves its acceptability to animals. However, feeding completely fresh cassava foliage to cattle and goats did not show any toxicity effect neither from CTs nor HCN, when cassava was managed as a semi-perennial forage with repeated harvests at 50 to 80 day intervals under fertilization (Seng Mom et al 2001; Seng Sokerya and Rodriguez 2001). Cassava foliage and cassava leaves have been used successfully as the sole diet for goats in Cambodia (both young and old leaves) without showing any negative effect from toxic compounds and with high intakes and digestibility (Theng Kouch et al 2003). Ffoulkes and Preston (1978) showed that the fresh foliage could be used as the sole source of protein and fibre for supplementing a liquid diet of molasses-urea for fattening cattle. In this case the growth rate was 800g/day. Seng Mom et al (2001) reported increases in daily weight gain in local cattle from 210 to 302 g/day when supplemented with fresh cassava foliage. Using cassava foliage made into hay is a popular feeding system for dairy cattle in Thailand. Wanapat et al (2001) indicated that supplementation with cassava hay reduced the need for concentrate, with no reduction in milk yield and increases in milk fat and milk protein. A further study in the same area reported that supplementation with cassava hay at 1 kg DM/day significantly improved total DM intake, DM digestibility and reduced the number of parasitic eggs in faeces of both grazing swamp buffaloes and cattle (Granum 2003). Seng Sokerya and Rodiguez (2001) recorded better growth and lower nematode parasite eggs in faeces when goats were supplemented with fresh cassava foliage as compare to grass.
In my research (Seng Sokerya et al 2003), the use of fresh cassava foliage as a forage supplement in basal diets of brewer's spent grains or wheat bran, led to better growth and reduced numbers of parasite eggs in faeces. Results were similar when cassava foliage was the only forage (50% of diet DM) or when it was mixed 50:50 with grass (ie: 25% of the diet DM). This result is strongly supported by the previous studies in the region (Netpana et al 2001; Seng Sokerya and Rodriguez 2001; Granum et al 2003) indicating the positive effects from using cassava foliage as a source of bypass protein and condensed tannins, thus providing beneficial effects to the ruminant in term of improving the production (milk and meat) and health in a system of organic animal production.
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