Abstract
The worldwide emergence of anthelmintic resistance against gastrointestinal (GIT) parasites prompts investigation towards sustainable alternative approaches. Accordingly, several approaches have been endeavored to control GIT parasites and increase economic values of livestock production systems. Current scientific evidence implies that there is substantial capability to use the plant bioactive compounds to enhance animal’s health and promote their productivity. Despite the great efforts in management, GIT parasites remain the main cause of mortality and weight gain–loss in ruminant industry. Recently, there is worldwide interest in exploiting plants bioactive and their secondary constituents as substitutes to anthelmintic treatment. However, we still necessitate to collect further data about their concentrations, sources, and composition, not only that but also understand their potential beneficial and detrimental impacts in livestock production. Simultaneously, our review discusses the research efforts towards the development of plants bioactive and their impact on GIT parasites elimination in ruminants. A summarized background on their impacts on ruminant productivity and the future research ppossibilities in this area were also provided.
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Introduction
The current livestock management operations and welfare integrity of food producing livestock in developing countries are facing many challenges to promote animal health and productions (Durmic and Blache 2012; Karki et al. 2018). In line with these constraints, the virtuous animal production has been boosted to meets the societal demands for agricultural food products and reducing the impact of livestock industry on the surrounding environments (Bickell et al. 2010). This notion entails less utilization of synthetic pharmaceuticals compounds, hormones, and in particular the routine use of infeed antibiotics (Piddock 2002). The detrimental impact and consequences of using the synthetics chemicals pave the way for development of other alternative and natural options to manage animal production (Zain-Eldin et al. 2013; Zein-Eldin et al. 2014). Currently, there is comprehensive curiosity in exploiting bioactive plants and their constituents, as alternatives to these chemicals (Pent and Fike 2018). While, bioactive plants and their metabolites have been exploited for centuries, we still require to congregate more data about their origins, concentrations, metabolism, absorption, and biological efficacy in order to determine their future benefit in improving animal health (Durmic and Blache 2012). Presently, there is a significant prospective to use the bioactive compounds (specifically tannin and saponin containing plants) to improve animal productivity, reproductive potency, meat quality, and control of GIT parasites infestation (Rochfort et al. 2008). Plants bioactive and their metabolites have been proved to be economical, efficient, easily available and safe to use with minimum side effect (Wijngaard et al. 2012; Ramírez-Rivera et al. 2010). Currently, there have been a remarkable number of plants and their bioactive constituents with anthelmintic activity stated (Salem et al. 2017). A web based search using the words ‘‘bioactive plants as anthelmintic’’, yielded over 1000 citations. While, the herbs-based anthelmintic were the main treatment for the GIT nematodes prior to advancement in pharmaceuticals drugs (Sandoval-Castro et al. 2012), their use are commonly restrained by the insufficient understanding of their authentic efficacy against specific parasites (Marie-Magdeleine et al. 2010).
In this context, our review summarizes the research efforts towards the role of plant bioactive and their metabolites on selected animal functions and their impact on GIT parasites elimination in ruminants. We also provided a summarized background on their impacts on ruminant productivity, and outlined the future research possibilities in this area.
Gastrointestinal parasites in ruminant
GIT helminthiasis has been defined as one of the significant health, welfare and economic issues in livestock production system notably in the developing countries (Waller 1997; de Mendonca et al. 2014). The primary risk factors of helminthiasis are generally relied to many factors including; host factors (Age and physiological status of the host), parasitic factors (different parasites epidemiology), and environmental factors (stocking rate, surrounding atmosphere, nutrition, and management protocols) (Tariq et al. 2008). GIT helminthiasis is a heterogeneous group of parasites with approximately 30,000 identified species. They are divided into phylum nemathelminthes (Roundworms: nematodes) and plathyhelminthes (flatworm: cestodes & trematodes). Approximately fifty percent of these species are considered marine parasites, twenty- five percent are free living, fifteen percent are animal parasites, and ten percent are plant parasites (Ghisalberti 2002). The most common GIT parasite species found in ruminants are listed in Fig. 1. In this group of parasites, Haemonchus contortus represent the commonly prevalent nematode in small ruminant that cause severe damage to their hosts., followed by Strongyloides, Trichostrongylus, Oesophagostomun, and Cooperia (Roeber et al. 2013). Most of these parasites are widespread in developing countries, and remains the main cause of increasing death rate, decreasing animal productivity (Zeineldin et al. 2018). Additionally, GIT Helminthiasis contribute to the prevalence of nutritional deficiencies, anaemia, eosinophilia, allergic manifestations and pneumonia in infected livestock (Tariq et al. 2009). Consecutively, animals have developed specific behavioral and physiological adaptations that neutralize this challenge and help in reduction the severity of parasitism. The infected animals at the pasture learn how to develop selective feeding behavior and self-medicate against GIT helminthiasis through increasing ingestion of plants bioactive with anthelmintic potential (Villalba et al. 2014). Comprehensive understanding of that mechanism in infected host will help researchers to invent suitable and more eco-friendly management strategies to enhance livestock health and productivity.
Alternative methods to limit gastrointestinal parasitism in ruminant
The traditional strategies for GIT parasitism control relies on the repeated use of conventional chemical medicaments (Hoste et al. 2006). The efficacies of chemical anthelmintic drugs against GIT parasitism have been reported with fluctuating accomplishment. The miss and overuse of these chemicals, increased prevalence of resistance in GIT populations, increased treatment cost and therefore increased economic impact of GIT parasites (Gárcia et al. 2016). Generally, the anthelmintic resistance is described as a heritable change in the ability of individual parasites to survive the prescribed therapeutic doses of an anthelmintic drug (Coles et al. 2006). The current prosperous application of helminthiasis control strategies was planned to reduce anthelmintic resistance in nematode populations. There have been various literature reviews on anthelmintic resistance that have archived the accessible data on the different types of nematodes to which resistance has been distinguished, to which anthelmintic it had created and in what area it has been found (Taylor et al. 2002; Waller and Thamsborg 2004; Coles 2005; Coles et al. 2006; Torres-Acosta et al. 2012). Responding to anthelmintic resistance crisis against the commonly used anthelmintic chemicals and the public health concern regarding utilization of synthetic therapeutics in livestock management systems, many research studies are designed towards alternative and natural approaches for GIT parasites (Marie-Magdeleine et al. 2010; Oliveira et al. 2017). These alternative strategies includes genetic resistance control, nutrition adjustment, biological control, vaccination, and pasture management techniques (Besier and Love 2003; Waller and Thamsborg 2004; Pisseri et al. 2013; Zeineldin et al. 2018). While, these alternative strategies are eventual option in maintainable GIT helminthiasis control in cattle, until now there is no suitable option to for nematodes control in sheep (Coles 2005). The challenge thusly is how to efficiently use a mix of these procedures to achieve the maximum anthelmintic control (Waller and Thamsborg 2004). In the meantime, there is a consistent need to develop new and alternative approach for GIT parasites elimination in ruminant, and to interface their utilization with enhanced control methodologies (Taylor et al. 2002).
Exploring the anthelmintic effects of plants bioactive in ruminants
The bioactive constituent generated by medicinal herbs to neutralize GIT nematodes are currently investigated and received a great attention in the field of anthelmintic medication (Athanasiadou and Kyriazakis 2004; Wolstenholme et al. 2004). The utilization of plants bioactive for their GIT helminthiasis counteractive action has its origin in ethnoveterinary traditional medicine. While, the anti-parasitic activities of plants bioactive and their metabolites has been generally based on episodic perception, there is as of now an expanding number of controlled experiments that aim to evaluate, quantify and validate such plant activities in a scientific manner (Marie-Magdeleine et al. 2010).
Throughout many years of researches, large number of plants bioactive with anthelmintic activities in ruminant has been scientifically approved in veterinary practice, either through administering plant extracts to the diseased animal or consuming the whole plant through feeding (Athanasiadou et al. 2007; Faria et al. 2016). Table 1 lists a selected example of these plants bioactive. Most of these studies have spotlighted on small ruminant under grazing conditions, in which animals were ingested freshly collected plants without further processing. For instance, Havardia albicans and Lespedeza cuneate were given to the sheep during feeding process as alternative for gastrointestinal parasite control (Galicia-Aguilar et al. 2012; Féboli et al. 2016). Notwithstanding, each year, the list of new plants with nematocidal in vitro and in vivo properties against known helminths is updated as new natural choices for supplanting (at any rate mostly) the utilization of synthetics chemicals. However these tremendous number of plants that have nematocidal activity, the majority of the bioactive constituents that responsible for this anthelmintic activity remain uncharacterized (Ghisalberti 2002). Exploring the in vivo and in vitro anthelmintic effect of the available plants bioactive and their secondary metabolites have been the subject of recent review (Zeineldin et al. 2018). The extent of described plants bioactivity shifts enormously and sometimes it is hard to evaluate the level of action since the compound that responsible for activity might be unidentified and the plant utilized as a part of the trials may have an unspecified amount of the bioactive constituents. The presumed bioactivity falls into an extensive variety of compound classes including; phenolics (tannins), lipids (fatty acids), alkaloids and terpenes (essential oils, saponins and glycosoylated triterpenes). It has been noticed that the synergistic impacts between the plant bioactive constituents especially lipids and essential oils is imperative for their natural biological activities and their nematocidal properties (Ghisalberti 2002). Similarly, recent studies focused on identifying the secondary metabolites that responsible for plants activity against GIT parasitism have identified a contributing role of the plants bioactive components including condensed tannins, catechins, polyphenolics, steroids, and flavonoids (Oliveira et al. 2009).
Tannins-containing plants are the commonly used plants bioactive, and their impacts on parasitic infestation have been the first to be explored among the known plants bioactive. Interdisciplinary groups of researchers (Paolini et al. 2003; Barrau et al. 2005; Alonso-Díaz et al. 2008; Vargas-Magaña et al. 2014; Hoste et al. 2015) have studied the role of plants containing condensed tannins in control of GIT helminthiasis particularly Haemonchus contortus. The condensed tannins biological mechanisms of action to eliminate parasites can vary from plant to another. Two main different mechanism of action have been suggested (van Zyl et al. 2017). Firstly, tannins-containing plants could act indirectly, by enhancing the reaction of the host to parasites. In view of their protein-restricting capacity, tannins can prevent breakage of proteins in the rumen and increase amino acid absorption by the small intestine, which thus enhance host homeostasis and modulate host immune response against different parasites (Min et al. 2003). Few studies have addressed this indirect mechanism by estimating particularly local or general parameters related to host immunity, but the outcomes remain to a great extent uncertain (Athanasiadou et al. 2005; Niezen et al. 2002; Tzamaloukas et al. 2005; Hoste et al. 2006). Secondly, the direct mechanism, in which, the tannin containing plants showed different anthelmintic potentials in themselves and influence several key biological processes of the parasites. This mechanism is bolstered by results from multiple in vitro tests and, importantly, from in vivo assays in small ruminant in which the short-term experimental design did not allow the development and expression of effective host immune reactions (Paolini et al. 2003; Athanasiadou et al. 2001).
Effect of bioactive plants on behavior, production and performance of ruminant
Generally, the plants bioactive have been approved to play a crucial role in increasing animal productivity, as well as in modification the animal behaviors (Table 2). The impact of bioactive compound on different physiological parameter in the host may be reversible or irreversible, acute or chronic, preventative, and or curative. Approximately, 80,000 plants bioactive are acknowledged for their importance in improving animal health and productivity worldwide (Bernhoft 2010). More recently, relationship between plant secondary metabolites and animal health has been the main point of scientific researchers to identify the specific plant components that have beneficial effect on animal production (Bickell et al. 2010; Stanner et al. 2004). More than 200,000 bioactive component are documented as plant secondary metabolites, with various categories including tannins, flavonoids, alkaloids, saponins, cyanogenic glycosides, non-protein amino acids, terpens, and glycosinolates (Hart et al. 2008). Considering the variation in the different structure and function of GIT between animal species, numerous investigations have exhibited that ingestion of plant secondary metabolites diminished feed conversion proficiency and impaired nutrient utilization (Reed 1995; Stienezen et al. 1996). While, others have revealed enhanced absorbability and feed effectiveness with bioactive compound use in food producing animals (Hussain and Cheeke 1995).
Effect of bioactive plants on animal reproduction
Bioactive plants may have beneficial outcomes in improving animal reproductive performance. The plant secondary metabolites can encourage expression of male conceptive practices, including mating and courtship behavior (Patel et al. 2011), increase production of sex steroids and increase sperm count (Gauthaman and Ganesan 2008). Additionally, high intake of plants bioactive that contains high amount of vitamin E connects with decrease prevalence of retained placenta and mastitis in ruminant (Celi and Gabai 2015).
Effect of bioactive plants on growth performance of animals
Plants bioactive represents an essential part in animal feeding and affect significantly growth performance and healthy status of animals. Plants bioactive demonstrated a significance contribution in the feeding of grazing animals especially in area where few or no choices are accessible (Mahala et al. 2007). Small ruminant used trees forages as a source of energy, vitamins, protein, and minerals. For instance, supplementation of Leucaena leucoephala to small ruminant gave higher convergences of rumen metabolites, which normally enhanced rumen capacity and absorbability (Bonsi et al. 1995). Most of the plant extracts are used to enhance growth performance and improve nutrient digestibility in food producing animals because of their beneficial impacts on ruminal microorganisms activity and amino acid flow to the GIT (Jiménez-Peralta et al. 2011). The plants bioactive and their constituents influence not only animal growth but also body structure and carcass composition. For example, natural plants bioactive, that consists of betaine (naturally occurring amino acid derivative) and conjugated linoleic acid can enhance the fat to lean content and has substantial implications on consumer acceptance (Sillence 2004).
Effect of bioactive plants on wool and skin quality
Plants bioactive can be utilized to heal skin wounds and mitigate skin bothering or aggravation, or to treat general skin disorders such as dermatosis, eczema, warts, and abscesses (Dilika et al. 2000). For example, sheep grazing on lotus containing tannins exhibited increased in wool production (Patra and Saxena 2011).
Effect of bioactive plants on immunity, stress and pain
Bioactive plants and their biological constituent have been demonstrated to boost and improve host function, with impacts extending from anti-inflammatory (Neto et al. 2005), to enhancing and modulation of humoral and cellular immunity (More and Pai 2011). For instance, ruminant grazing on plant rich in bioactive constituent showed elevated in immune response with lower level of lymphocyte, monocyte and eosinophil (Tzamaloukas et al. 2006; Mahgoub et al. 2008). Moreover, plant secondary components have showed a great effect on the host psychological and physiological response (Stafford et al. 2008). For instance, feeding Lavender oil (Lavendula augustifolia) to the small ruminant resulted in diminish anxiety-like behavior (Hawken et al. 2012). While, other plants bioactive (Passiflora incarnate, chamomile, Matricaria recutita, and Papaver somniferum) were used traditionally to calm horses and donkeys (Cruz-Vega et al. 2009).
Further consideration when using the plant bioactive
However the existing knowledge on anthelmintic effect, and the beneficial effect of plants bioactive in improving host productivity, the in-field toxicity and environmental risk should be assessed before introduction of any new feed as alternative to the current used strategies (Hoste et al. 2006). Additionally, the variations between the gut anatomical structures and GIT different prevailing conditions could play a crucial role in the response of GIT parasites to plants bioactive (Hoste et al. 2006). The host physiological adaptations to plants bioactive constituent could change the amount of bioactive components needed to interact with the parasites (Silanikove 2000). There are additionally a few variables which should be considered while surveying the effect of bioactive plants in livestock producing system. For example, the ethnoveterinary medicines are usually produced either from the entire plant, or from part of the plant. The field application of plants bioactive are often lack standardization, because they have been used in livestock through trial-and-error, instead of valid scientific approach. Therefore, isolation and distinguishing of the plants bioactive biological compounds is critical (Provenza and Villalba 2010). Another important factor that should be considered is the palatability of bioactive plants (Rogosic et al. 2008). Generally, plants bioactive are considered unpalatable, which in turn reduced animal consuming ability (Beauchemin and McGinn 2006). Further factors, for example, administration time (the time it takes to achieve the advantageous effect), persistence, adaptation, and interactions with host should be likewise considered. It is important to conduct a long term and controlled experimental studies with repeated applications of the plants bioactive to allow adequate time and amounts for the bioactive effect to develop, but also to give the host the chance to adapt the plants bioactive components. Finally, the future use of bioactive plants needs to consider the different environmental issues such as agronomy of the plant, accessibility of natural resources, preservation of resources and ecological sustainability. Utilization of bioactive plants in livestock production systems must be well-founded and linked to farm economics, to clearly demonstrate the improvement percent in animal health without affecting total farm productivity (Durmic and Blache 2012).
Concluding remarks
This review article aimed to cite the widely used plants bioactive for treatment of most common GIT parasites in ruminants and to document scientist’s interest in utilizing natural option as alternatives to the synthetics chemicals in the livestock production industry. Several research studies in ruminants to date have investigated the use of specific classes of plants bioactive for nematocides treatment, suggesting that this could be a fertile area for future research. Despite that, assessing the potential anthelmintic effect of plant bioactive lack the chemical analysis of plant constituents. Considering the previously mentioned issues, this review suggests that plants bioactive may certainly be valuable for livestock health, while in the meantime, highlights the need for further in-depth and controlled in vivo studies to validate and assess the plants bioactivity. Isolating plant bioactive compounds is vital to understand the bioactive components and their mechanism of action to achieve maximum efficacy of the plants and reduced their potential toxicity. Exploiting plants bioactive in livestock management system may offer practical, inexpensive, environmentally safe, and sustainable alternatives to synthetic chemicals, however more research is required before such compounds can be suggested in commercial livestock production systems.
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Zeineldin, M.M., Sabek, A.A., Barakat, R.A. et al. Potential contribution of plants bioactive in ruminant productive performance and their impact on gastrointestinal parasites elimination. Agroforest Syst 94, 1415–1432 (2020). https://doi.org/10.1007/s10457-018-0295-6
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DOI: https://doi.org/10.1007/s10457-018-0295-6