ReviewPlant bioactives for ruminant health and productivity
Graphical abstract
Plants can be used to enhance animal health. Research on ruminant specific treatments reinforces the importance of understanding phytochemistry. For example, researchers have recently demonstrated that saponins with different core structures (1 and 2) have disparate effects on methane production. Plant use for animal health is analysed in this review.
Introduction
Mainstream animal production relies heavily on the use of pharmaceuticals. Many of these products are developed through research and development for human pharmaceutics. Natural products are an important source of new drugs and drug leads in the pharmaceutical industry. For the animal market many of the currently used antimicrobial, feed additive antibacterial, endectocide and anticoccidial drugs are either natural products or synthetics based on natural products (Ruddock, 2000). The majority of these natural products are produced from the fermentation broth of microorganisms, though plants have also been an important source of bioactives. There is increasing public concern regarding the use of pharmaceuticals in the animal industry. Much of this has been as a result of the emergence of drug resistance. A particular area of criticism has been in the use of antibiotics as growth promoters and the associated risk of developing antibiotic resistance in human pathogens (Barton, 2000). This is not a new issue and in 1969 the Swann report resulted in the withdrawal of β-lactams from feed in the UK (Ruddock, 2000). However, this increasing trend has led to a closer examination of plants for animal health. In Western culture, plants in the livestock industry have largely been considered as a source of nutrition or potential source of toxicity. Increasingly there is the realization that plants may offer non-nutrient performance enhancing factors that benefit animal production (Greathead, 2003). This realization has resulted in increased research, with the number of publications in this area increasing over the last 8–10 years. The research area is of sufficient significance to warrant focus in the journal ‘Animal Feed Science and Technology’. In 2005, issues one and two were dedicated to “Phytochemicals in Livestock Production Systems”. Specific programs to investigate the use of plants for animals have also been developed. For example, the banning of feed antibiotics by 2006 in the European Union (EU) prompted investment in the Framework 6 REPLACE program which, aims to screen 500 plants for a range of activities, including antibacterial, nematocidal and immune stimulating effects (EU-Replace, 2006).
This paper reviews the use of plants or their extracts to enhance ruminant health. Evidence from various sources, including in vitro and in vivo experiments and ethnoveterinary studies is discussed. Not considered here are potential natural products derived from organisms other than plants. That is, bacteria and fungi are not covered in this review. There is already substantial evidence for the success of microbes in this area, and indeed, many of the antibiotics and helminthics used today are either microbial natural products or derivatives there of (e.g. avermectins and milbemycins from Streptomyceses species). Live organisms such as fungi have also been used for in situ nematode control. The commercially available DiTera contains the fungus Myrothecium spp whilst Paecil, which contains Paecilomyces lilacinus, has been used as a soil drench, the fungus being a nematode egg parasite (Ghisalberti, 2002). Potential biological mechanisms of control, such as this, will not be considered further in this review.
It is worth noting that plant bioactives are still an under-explored area of research and in many cases although biological activity has been observed, the natural phytochemicals responsible for the activity have not been identified. For example, a compilation of plants with nematocidal activity produced in 1997 contained 150 entries and for most the active agents have yet to be identified (Ghisalberti, 2002).
Animal pharmaceutics are often derived from studies for human medications and for these studies ruminants are usually not the focus of bioactive investigation. There have been an extraordinary number of plant metabolites with antibiotic activity reported. A literature search using the terms “antibiotics from plants”, yielded over 5000 references. The majority of the compounds/plants identified in these articles will never have been specifically tested in ruminants. Indeed, adding the words “and studies in ruminants” reduces the number of references to 30, and only a small proportion of these is relevant to the topic. There is no doubt that past knowledge and the literature is a useful guide for developing therapeutic approaches. However, even a cursory search of the literature reveals a daunting amount of information on plant metabolites but with relatively little work done for ruminant health. Table 1 presents a summary of the results of a literature search that examines specific classes of plant compounds. Plant metabolites were searched based on structure type (terpene, alkaloid, lipid, carbohydrate, aromatic, saponin, tannin) and then each class examined for reports of bioactivity, specifically antibiotic or anthelmintic activity. The results were further refined to focus on ruminant specific research. There are some limitations and redundancy in this data but it highlights the large number of publications discussing plant metabolites and their antibiotic and anthelmintic activities. Manual inspection of each refined reference further reveals that some of the articles are ‘false positives’ in that they do not necessarily focus on ruminant health (e.g. some mention bovine serum albumin in the abstract). Fig. 1 portrays this information visually and shows the areas of greatest study in terms of ruminants. Indeed, for ruminants, there is very little literature that focuses on plants as alternatives to antibiotics. In ruminant health the focus has been on bioactive effect of plants on ruminal flora rather than on specific pathogenic bacteria. This is perhaps understandable, since many of the desirable effects of antibiotics used as growth stimulants act through modification of the ruminal microbe population.
Delivery of bioactives is an important consideration. The form the bioactive presented to the animal will affect not only bioavailability but also cost of delivery. Options for delivery range from growing the plant in field, through to application as hay, to dosing with either pure material or concentrated plant extract. In many ways the simplest of these is infield plant production, however there are numerous considerations as highlighted in a recent review, “Arguably the simplest method of delivering bioactive plant secondary metabolites to animals outdoors would be to grow the relevant plants in a field and then let the animals graze them in a controlled manner, assuming they are palatable” (Greathead, 2003). However, the authors note that the efficiency of such a method is doubtful, since despite the crude control of intake via controlled grazing, there would be no control on dosage due to the interplant variation in secondary plant metabolite (SPM) content. Methods of uniformly stressing plant crops to ensure uniformity of SPM and perhaps even invoking the production of certain metabolites could be investigated (Greathead, 2003). Plants are essential for ruminant nutrition but offer benefits beyond basic nutrition. Judicious use of specific bioactive plants has the potential to impact on almost every aspect of ruminant production.
Section snippets
Feed intake and behaviour
Feed intake and animal-feeding behaviour is governed by many factors including availability, palatability and feed back mechanisms. Tannin containing plants have been the subject of significant research effort. The recent review by Mueller-Harvey (2006) is an excellent summary of this work. Condensed tannins may be beneficial in the diet but at certain levels begin to affect feed intake. This level varies considerably, depending on the chemical nature of tannin and the animal species studied.
Bacterial populations
Antibiotic activity is one of the simplest and most important bioactivities to test for and there is a large body of literature reporting on research in this area. Plants have long been a rich source of antibiotics and an extraordinary number of plant metabolites with antibiotic activity have been reported. The majority of plant-derived antibiotics tested specifically for ruminants are tested in order to assess the effect on the ruminal flora. The aim is generally related to safety (since
Nematodes
Nematodes are a diverse group of organisms with some 30,000 described species. Approximately 50% of these are marine, 15% are animal parasites, 10% are plant parasites and 25% are free living (Ghisalberti, 2002). Anthelmintic resistance in GI nematodes is an increasing problem, though modern pasture management techniques including pasture rotation, harrowing, regular manure removal, and ‘worm and move’ programs can be of help in parasite control (Besier and Love, 2003, Nguyena et al., 2005). It
Potential delivery mechanisms of bioactive compounds to animals
The potential delivery mechanisms range from a purified plant bioactive (in a capsule or injectable form) to in situ grazing on plants in the paddock. In between these extremes are options such as:
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Drenching with partially purified and concentrated plant extract
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Drenching with crude plant extract.
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Incorporation of processed crude plant material or extract into feed pellets or solution
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Application of fresh plant material to the paddock/feed lot
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Application of partially processed plant material to the
Safety and environmental considerations
The anti-nutritional activity of tannins is well documented but the potential negative effect of many substances has not been investigated in any detail. Before the introduction of any new feed, in-field toxicity and nutritional effects must be evaluated. The outcomes of such studies may also suggest the best way to deploy the bioactive containing material. For example, if in situ feeding of the plant proves to be detrimental, the plant may still be of use for supplemental feeding where the
Social drivers for the replacement of antibiotics in animal feed
Human health and safety concerns are ultimately behind the push to reduce the use of antibiotics in animal production. There is increasing public concern regarding the use of pharmaceuticals in the animal industry. Much of this has been as a result of the emergence of drug resistance. A particular area of criticism has been in the use of antibiotics as growth promoters and the associated risk of developing antibiotic resistance in human pathogens, though there is still considerable debate about
Regulatory frameworks
Animal feed is subject to regulation in many countries including the United States, the European Union and Australia.
Current research programs
There are two large EU programs aimed at developing practical alternatives to antibiotic use in animal feed and replacing the use of synthetic antibiotics in animals (EU-Replace, 2006). These are large-scale projects involving 7–10 member countries and are well funded.
Conclusion
The use of plant bioactives for animal health is an area of increasing research importance. Many of the studies in ruminants to date have targeted specific classes of bioactives such as tannins and saponins. The focus of most ruminant research has been on ruminal flora modification for a reduction in methane emission and enhanced growth. The manipulation of meat and milk quality, particularly with respect to fatty acid composition, is an active area of research. Feeding or supplementation with
Acknowledgment
This work was financially supported by the Meat and Livestock Australia Limited (MLA).
Simone Rochfort completed her PhD in marine natural products chemistry at the University of Melbourne in 1996. After a postdoctoral fellowship with Dr. Jeffrey Wright, National Research Council of Canada, she returned to Australia to take up a research position with AstraZeneca and Griffith University where she worked the discovery of natural products for human pharmaceuticals. Dr. Rochfort’s research in the pharmaceutical and biotech industries continued until 2004 when she joined the
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Simone Rochfort completed her PhD in marine natural products chemistry at the University of Melbourne in 1996. After a postdoctoral fellowship with Dr. Jeffrey Wright, National Research Council of Canada, she returned to Australia to take up a research position with AstraZeneca and Griffith University where she worked the discovery of natural products for human pharmaceuticals. Dr. Rochfort’s research in the pharmaceutical and biotech industries continued until 2004 when she joined the Victorian Department of Primary Industries. She is currently employed as a Principal Research Scientist and applies her natural products research interests to metabolomics and the substantiation of functional foods.
Anthony Parker graduated with a B.App.Sc in animal production from the University of Queensland. He received his Ph.D. in animal physiology from James Cook University in 2005. He has worked as a ruminant nutritionist and animal production consultant in the dairy, beef and sheep industries in Australia. He is currently employed by Ridley Agriproducts Pty. Ltd. as a product development manager.
Frank Dunshea received his B.Agric.Sci. (Hons.) and Ph.D. degrees from La Trobe University in Melbourne Australia in 1983 and 1988, respectively. His Ph.D. research was on fat metabolism in the undernourished and lactating goat, and was directed by Professor Alan Bell. After a postdoctoral fellowship with Professor Dale Bauman at Cornell University he returned to Werribee, Australia to work in government-funded research. His research focused around the interactions between human and animal nutrition and the use of domestic animals in nutritional and biomedical research, particularly in the areas of functional foods and bioactives. In 1994, he was the inaugural recipient of the Nutrition Society of Australia Research Award and in 2004 was awarded the Daniel McAlpine Outstanding Achievement Award for Innovation in Agricultural Research for his biomedical and functional foods research. In 2006, He was appointed as the Chair of Agriculture at the University of Melbourne where he continues to work in the area of plant and animal bioactives.