Nutritional strategies for small ruminant gastrointestinal nematode management

Abstract

Pasture management can reduce the risk of gastrointestinal nematode infections in small ruminants and enhance the nutritive value of their diets. Supplementation, notably with protein, can increase the resistance and resilience of small ruminants to gastrointestinal nematodes. Copper oxide wire particles can reduce barber pole worm (Haemonchus contortus) infections in small ruminants and increase the efficacy of dewormers. Plants rich in condensed tannins can be an ally to sustainable integrated parasite management by controlling gastrointestinal nematodes and improving feed efficiency. Gastrointestinal nematodes (GIN) are the most important health issue for small ruminants in many world regions. The GIN parasitism causes welfare concerns and severe economic losses related to reduced productivity, cost of treatment, and, eventually, mortality. The most economically significant GIN in small ruminants belongs to the order Strongylida and the family Trichostrongylidae. They are found in different parts of the digestive tract according to the species. Barber pole worm (Haemonchus contortus) and brown stomach worm (Teladorsagia circumcincta), bankrupt worm (Trichostrongylus colubriformis), and nodular worm (Oesophagostomum columbianum), which are frequently associated with parasitic gastroenteritis, colonize the abomasum, small intestine, and large intestine, respectively. Barber pole worm is by far the most common and pathogenic GIN of small ruminants in tropical and subtropical regions due to the blood-feeding habit (chiefly linked to anemia; Figure 1) and high prolificacy, as a female can lay from 5,000 to 10,000 eggs per day. Goat with severe anemia caused by barber pole worm (Haemonchus contortus). The pale to white conjunctiva, weakness, lethargy, and sudden death are clinical signs of hemonchosis. Brown stomach worm is a major parasite species in temperate countries. Bankrupt worm invades the intestinal mucosa and causes lesions that develop as circular thickened areas several centimeters in diameter, while nodular worm larvae penetrate the large intestinal wall and become encysted, forming multifocal nodules throughout the lower gut. How do gastrointestinal nematodes infect small ruminants? During the parasitic phase, adult worms live in the animals. Their eggs are shed in the animal’s feces, contaminating the pastures. The animal infection occurs via ingestion of larvae present in contaminated forage. The control of GIN in small ruminants has mainly relied on using anthelmintics. With the failure of chemotherapy due to widespread parasite resistance to commercially available anthelmintics (Charlier et al., 2022) and concerns about drug residues in foods and ecotoxicological effects of drug excretion on the environment, researchers have studied other tools for integrated parasite management (IPM; Burke and Miller, 2020). Feeding a balanced diet for maintenance, growth, and reproduction directly influences health since host resistance to infection is mediated predominantly through the involvement of its immune system (Atiba et al., 2020). Manipulating diets can be an essential tool to increase small ruminant resistance and resilience to GIN (Coop and Kyriazakis, 2001; Hoste et al., 2016). Resistance is the ability to prevent or limit establishment or development of infection. Resilience is the ability to maintain a reasonable production level when subjected to a parasitic challenge. This article examines nutritional strategies as tools for small ruminant GIN management. First, we will uncover the impacts of GIN parasitism on nutrition and metabolism. Then, as most of the small ruminants are raised on pastures and get their nutrients from the forage plants, we will look at pasture management impacts on GIN parasitism and forage nutritive value. Following, we will describe how protein, energy, mineral, and vitamin supplementation can affect the host resistance and resilience. Next, we will discuss how the use of copper oxide wire particles (COWP), a dietary supplement, can control barber pole worm. Finally, we will explain how plant secondary compounds can be incorporated into small ruminant diets and contribute to IPM. The different components of feed systems presented in this article are related to nutrition and interact with GIN management with the main goal to limit gastrointestinal parasitism in small ruminants by minimizing contamination of pastures and the contact of hosts with the infective third stage larvae, eliminating or disturbing the biology of GIN in the host, and improving host response (resistance and/or resilience; Torres-Acosta and Hoste, 2008). The primary pathophysiological effects of GIN on nutrition and metabolism that impair small ruminant production are reduction of voluntary feed intake, decreased feed efficiency, and changes in nutrient utilization (Hoste et al., 2016). A reduction of intake from 10% to 30% is commonly observed in subclinical infections (Coop and Sykes, 2002). Reduced feed intake directly impacts the level of nutrients ingested and, therefore, the animal response and function. Loss of endogenous protein into the digestive tract due to leakage of plasma protein and increased mucoprotein can be substantial in parasitized small ruminants, exemplified by 10% loss of circulating blood per day in barber pole worm and 20 to 125 g protein per day in bankrupt worm infections in sheep (Coop and Kyriazakis, 2001). Blood losses can be much more significant than the blood consumption itself as barber pole worm uses the lancet to cut the abomasal tissue that induces hemorrhages. As a result, haemonchosis in sheep and goats can induce hematological alterations (hypoproteinemia, hypoalbuminemia, and hypoglobulinemia), anemia, and depletion of serum macro and trace minerals (e.g., P, Ca, Fe, Zn, and Cu; Coop and Sykes, 2002; Hoste et al., 2016; Atiba et al., 2020). Parasitized animals not only have their digestion impaired due to the reduction of enzymatic functions and changes in digestive juice secretion but also suffer a decrease in nutrient absorption in the small intestine as a result of disrupted digestive process. Ultimately, nutrients are diverted from tissues (e.g., muscle, udder, wool follicles) to compensate and replace losses caused by GIN (Coop and Sykes, 2002; Athanasiadou et al., 2008). The allocation of absorbed nutrients varies according to the order of priority, depending on the physiological stage of the animals, such as growth and reproduction (Coop and Kyriazakis, 1999). In all physiological stages, maintenance of body protein, including repair, replacement, and reaction to damaged or lost tissue, is the number one priority (Figure 2). Possible ordering of priorities (1 highest to 4 lowest) given by a growing or a reproducing animal to its various body functions when partitioning a scarce food resource. For a naive, growing animal without any prior experience of a gastrointestinal nematode challenge, the phase of acquisition of immunity is considered separately from that of expression of immunity. Maintenance of body protein includes repair, replacement, and reaction to damaged or lost tissue. Source: Adapted from Coop and Kyriazakis (1999). As the allocation of nutrients to reproduction (pregnancy/lactation) is prioritized before the expression of acquired immunity, peri-parturient rise occurs, which is the rise in fecal parasitic output due to relaxation of acquired immunity to parasites around lambing/kidding (Coop and Sykes, 2002). The depletion of intake, digestibility, and nutrient utilization, and consequently animal performance, depends on several factors related to both parasites (i.e., species and number, extent of larval challenge) and host (species, breed, age, physiological state, nutritional and immune status; Coop and Sykes, 2002; Athanasiadou et al., 2008; Hoste et al. 2016). Nutrition strategies in a small ruminant IPM program should be seen in a holistic approach, in which its effects on host-parasite interaction are not isolated (Figure 3). First and foremost, pasture management and complementary forages can help to reduce the risk of GIN infections and provide good forage quality. Furthermore, pasture management can potentially increase soil organic matter and sequestrate carbon. Then, supplementation, which can reduce fecal egg counts (FEC; the gold standard to estimate worm burden in the live animal) and adult worm burdens, and increase performance. Among minerals, we highlight the use of COWP to control barber pole worm infections and increase the efficacy of dewormers. Finally, the inclusion of plant secondary compounds in sheep and goat diets (e.g., condensed tannins) as an ally to manage GIN, improve feed efficiency, and decrease methane emissions. Nutritional strategies for small ruminant gastrointestinal nematode management. Pasture management (species, variety, environment, soil fertility, grazing system, defoliation frequency and intensity, and forage allowance), complementary forages (small grains, summer annuals, browsing, hay, silage, haylage, and agricultural byproducts), supplementation (protein, energy, minerals, and vitamins), copper oxide wire particles (COWP; dose, and frequency) and plant secondary compounds (present in legumes, herbs, shrubs, trees, and among others) affect nutrition. Nutrition (feed composition, digestibility, and intake) influences animal response (age, breed, natural resistance, production level, and physiological stage) to worms (species, number, and extension of the challenge), increasing resistance (by decreasing fecal egg counts and worm burden), and resilience (hematocrit and performance). Grazing management is a crucial point in a sustainable IPM program because pastures are where most of the worms are located, in the form of eggs and larvae. We cannot dissociate the impacts of pasture management on larvae ingestion and forage nutritive value. Rotational grazing allows producers to control stocking rate, how short plants are grazed, how long animals graze in a paddock, and grazing intervals in order to reduce the ingestion of infective larvae (Glennon, 2017; Burke and Miller, 2020; Bricarello et al., 2023). Rotational grazing also can provide forage with high nutritive value, impacting positively the host’s immune response. Co-grazing small ruminants with cattle and horses can reduce parasite transmission, as cross-infection usually has little significance (Bricarello et al., 2023). Complementary forage plants also can contribute to a sustainable IPM. Incorporating annual forages into a pasture-based production system can reduce the risk of parasite infection in multiple ways. Warm- (e.g., pearl millet and Sudan grass) and cool-season (e.g., oats, rye, triticale, and wheat) annuals are known for their high nutritive value and can meet the energy and protein requirements of many classes of small ruminants. In addition to higher nutritive value compared to perennial grasses, planting these annuals will result in 45 to 60 days of plant growth before grazing, which reduces larvae availability (notably when there is some level of soil disturbance) and lowers the chance for the animals to ingest infective larvae when correctly managed (Glennon, 2017). Legumes and brassicas also are good options of complementary forages for small ruminants. Allowing animals to browse on woodlot vegetation encourages them to eat higher in the canopy, where there is less chance of picking up parasites. Additionally, it can be used as a strategy to rest permanent pastures and provide an additional feed source while warm-season forages are growing. In silvopasture systems, which is the practice of integrating livestock, forage production, and forestry, it is possible to provide high-quality forage and plant secondary compounds while keeping animals from continuously grazing close to the ground (Glennon, 2017; Griffiths and Carr, 2022). This alternative is more suitable for goats, as they are browsers, than sheep, that are grazers. Because of inherent grazing behavior, goats seem to develop a lower immune response against GIN than sheep. In predominantly grass pastures, exposure to GIN larval challenge causes higher levels of infections in goats than sheep, differentially when the animals have the opportunity to browse (Hoste et al., 2008). Protein has been understandably the most studied nutrient in supplementation programs aiming to increase resistance and resilience of small ruminants to GIN due to its importance in repairing damaged tissues, offsetting endogenous protein losses, and its role in the host’s immune response (Coop and Sykes, 2002). Protein supplementation can influence the different effector mechanisms of the immune response towards GIN such as proliferation of inflammatory cells (i.e., mucosal mast cells, globule leucocytes, eosinophils and goblet cells), associated release of highly proteinaceous effector molecules (e.g., mast cell proteases, leukotrienes, and mucoprotein-containing mucous), and production of immunoglobulins (e.g., IgA and IgE; Athanasiadou et al., 2008). Additionally, protein supplementation seems to improve host resilience by diverting metabolizable protein toward dealing with the detrimental effects of the infection and thus improving animal production and reproductive performances (Atiba et al., 2020). High-protein diet (20% of crude protein) reduced brown stomach worm burdens in single- and twin-bearing ewes compared to low-protein diet (12% of crude protein), regardless of the level of dietary energy (low 70:30 vs. high 30:70, alfalfa hay:ground barley; Figure 4). Average brown stomach worm (Teladorsagia circumcincta) burdens (geometric mean log10x + 1) of single- and twin-bearing ewes fed low- and high-protein and energy diets. Regardless of the level of dietary energy, increasing protein in sheep diets increased resistance to brown stomach worm by reducing 80% of worm burden. Source: Adapted from Donaldson et al. (1998). Increased protein in sheep diets during the early period of infection can influence the later stages of development of resistance and resilience to barber pole worm (Datta et al., 1999) and bankrupt worm (Kahn et al., 2000). Interestingly, feeding sheep a more proteaceous diet for a relatively short period (i.e., 9 weeks) can result in long-term benefits (i.e., over a year), probably due to enhanced immuno-responsiveness to GIN (Datta et al., 1999). Supplementation can be used as a tool to boost the immune response in critical phases of small ruminant production, for instance, to reduce peri-parturient rise (Kahn et al. 2003) and post-weaning mortality (Coop and Kyriazakis, 2001). The protein levels in relation to maintenance requirements and the demand for other physiological functions influence the potential for protein to enhance resistance to infection. However, the magnitude of improved host resistance following protein supplementation depends on the degree of protein scarcity in the absence of supplementation (Kahn et al., 2000). Different protein feeds may reduce GIN infections and increase animal performance. For instance, fish meal supplementation can offset hypoproteinemia of predominantly barber pole worm parasitized sheep and significantly affect immunological responses indicated by FEC reductions and increased hematocrit and growth performance (Crawford et al., 2020). Supplementing sheep with soybean meal increased resilience, with fewer clinical signs of haemonchosis (i.e., anorexia, hypoproteinemia, hypoalbuminemia, weight loss, and edema), and resistance, with lower FEC and worm burdens (Wallace et al. 1995, 1996). There is an interaction between nutrition and genetics on the host’s immune response, in which breeds or selected lines more resistant to GIN do not respond to protein supplements to overcome the adverse effects of parasitism as well as less resistant ones (Wallace et al. 1995, 1996; Khan et al. 2003). The production level is another factor that affects the response of protein supplementation on resistance and/or resilience to GIN infections. Etter et al. (2000) found that low- and high-milk-producing goats infected with bankrupt worm had lower FEC when they received high protein diets (130% of the requirements), suggesting that resistance was enhanced by protein supplementation; however, only in high-producing does, the milk production and milk composition parameters were improved with high-protein diet. Energy supplementation may also affect the resistance and resilience of small ruminants to Supplementing goats, infected with GIN and with of the body weight of ground of energy and of protein increased resistance (i.e., decreasing worm bankrupt worm burden and barber pole and bankrupt worm and resilience (i.e., increasing growth of the animals compared to additional per et al., As supplementation is an to be by the will be on the challenge, animal’s forage availability and and Grazing infected with barber pole worm fed with highly proteinaceous of crude protein), with soybean meal and at a level of increased growth performance, and hematocrit while reduced compared with mainly when predominantly pastures compared to pasture from et al., to these the in growth by in days supplementation and in per in supplementation crude protein and metabolizable at the level of increased resistance (i.e., decreasing the of and resilience (i.e., increasing growth performance and wool of grazing infected with GIN, compared with ones et al., 2022). to replace of and of soybean meal not the when the composition the of the immune system the of several and trace The of minerals for animals are is for animals an immunological challenge (Atiba et al., 2020). to these supplementation of and can enhance host resistance against nematode as by decreased FEC and worm and vitamin supplementation decreased FEC and increased energy utilization and a tool to be in for controlling GIN in small ruminants et al., 2023). The COWP are a dietary that an alternative to since they and Miller, 2020). The COWP are as a (Figure and are only against barber pole not intestinal Copper oxide wire particles (COWP), g COWP have against abomasal nematodes. The COWP on adult nematodes through the increased copper of the host, or directly due to increased copper in the abomasum, which potentially and penetrate the of barber pole worm and Miller, 2020). The COWP are in The is to the animal using a to g is for and while for ewes and the varies from to in substantial FEC reduction days and Miller, 2020). A of g in infected sheep and goats FEC by and and barber pole worm burden by and days et al., the of COWP not more than to the but animals can be 4 to on signs of There is known parasite resistance to and its use the efficacy of the anthelmintics and and Miller, 2020). However, as sheep are to copper which can result in is that copper levels be and the The of COWP may be in with a and feeding or grazing a forage rich in condensed tannins and Miller, 2020). The plant secondary compounds with and of depending on the can reduce feed intake, induce nutritional and effects and Miller, 2020). However, when used in or when to exposure to GIN or plant secondary compounds have the potential for controlling GIN in small ruminants (Hoste et al., et al., The of these compounds that has received the most is condensed tannins and Carr, 2022). Plants rich in condensed tannins with against GIN in sheep and goats among (Hoste et al., 2016; et al., tannins can have and effects on The effects are associated with the of larval which egg larval and while effects are associated with to protein metabolism and immune the animal (Hoste et al., et al., 2020; Griffiths and Carr, 2022). and sheep fed hay, and decreased larval and worm burdens, potential to be used in an when dealing with barber pole worm However, feeding (i.e., weeks) can to the of some trace minerals, reducing their availability to the the condensed tannins the in the such as and which can increase feed et al., 2020; et al., to the in the energy loss in the digestion and it is an as the most critical related to ruminant Nutrition is an essential tool in a sustainable IPM program for small ruminants, to increase resistance and resilience when animals GIN Pasture management and the use of complementary protein, energy, minerals, and supplementation; utilization of and the inclusion of plant with secondary compounds (e.g., condensed tannins) in the diets are nutritional strategies that producers should to overcome gastrointestinal infections in sheep and should how to the different nutritional strategies in feeding systems and their effects on animal more GIN animal performance, and and of small ruminant is an and small ruminant at the of of received and degree in animal from in a degree in systems from the in the and a degree in from in Additionally, has at the of and program at is to and to develop sheep and goats value using multiple extension to increase and of small ruminant production, and is a of the for Burke is a animal in the of received a in reproductive biology at a in animal from the of and a degree from in the Burke has been with since where has on the control of gastrointestinal nematodes in sheep and program on organic and production systems for small ruminant producers and includes development of to anthelmintics such as and for parasite resistance, nutrition and copper oxide wire is one of the of the for We from the of of for the The and in this are of the and should not be to any or or of or in this is for the of and not or by the is an opportunity and to and for the in Figure which is by The in this are of the and do not the or of the or the Burke was a for this issue of This had on the and the

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