D.H. Machin
Dr David Machin is an independent consultant in feed resources and livestock production, based in the United Kingdom.
The safe use of plant and animal by-products is an important means of disposing of materials that could otherwise be potential health and environmental risks and, at the same time, obtaining value from their use. This article considers the different approaches that countries take to feed safety as well as the main issues associated with the safe use of some of the most significant animal and plant by-products. In particular, the article concentrates on the implications of bovine spongiform encephalopathy (BSE) on animal carcass waste and swill processing, as well as on poultry waste use. The main problems associated with the use of plant by-products, including aflatoxins, antinutritional factors, toxic amino acids and alkaloids, are discussed and approaches to detoxification described. The conclusion is that all countries need to establish strong, scientifically based regulatory means of controlling and monitoring the use and processing of these by-products, in order to minimize potential breakdowns in animal and human health.
Degree of intensification of the animal industries
Wealth and its distribution within the country
Public awareness of food issues
Degree of regulation of the animal production and animal feed industries
Per capita consumption of animal products
Overwiew of the safe use of plant and animal by-products
The safe use of by-products as animal feeds is an essential means of utilizing many materials that would otherwise be of little economic value and could incur disposal costs or become environmental pollutants. However, because of unbalanced nutrient compositions and the possible presence of toxins and pathogens or antinutritive factors, the use of by-products can easily pose a threat to consuming animals and, in turn, consuming humans.
The subject of animal feed safety has become a major concern in recent years, following the loss of public confidence in the livestock industry. This has been brought about by events such as the bovine spongiform encephalopathy (BSE) crisis in the United Kingdom and the rest of Europe, dioxin in feeds in Belgium, the use of genetically modified organisms (GMOs), aflatoxin contamination of many feed ingredients and the presence of Salmonella spp. in eggs and meat products worldwide. Estimates based on World Health Organization (WHO) statistics suggest that hundreds of millions of people worldwide suffer from diseases contracted through food consumption, and that developing countries suffer the most (Saucier, 1999).
In order that the people who consume animal products produced from by-products can do so with confidence, it is essential that there is a profound scientifically based understanding of the dangers of using all such materials and of ways in which they can be made safe. At the same time, it is important that monitoring and regulatory agencies in countries where such materials are fed are aware of the issues involved and have appropriate systems in place to process and regulate the safe use of all these materials.
Around the world, there are enormous variations in approaches to the safe use of any feedstuff, including by-products. This is a reflection of the disease status, the economic status and the degree of public awareness of such issues in different countries.
At the upper extreme are the countries of Western Europe and North America, which have very intensive animal industries. In general, these countries have good animal disease status, populations that are relatively wealthy and a high degree of public awareness about animal product safety. As a result, the animal products produced in such countries are generally of high quality and represent a low risk to the consuming public. Such countries also have a high degree of regulation but waste considerable amounts of potentially high-quality material of relatively low risk to public health in order to try to eliminate all risk.
At the opposite extreme are the poor countries of Africa and Asia, which have largely extensive animal industries of poor health status, relatively poor populations and a low level of public awareness about animal product safety
From this description it is clear that the main issues relating to a country's human food safety include:
Each of these key issues is discussed in a separate section of this article.
It may be expected that diseases are likely to be most common in intensive production systems. However, in most cases, diseases are generally better controlled in such situations than in extensive systems. This is principally a result of large intensive industries being able to justify high-tech facilities, more staff and better feeding and health management.
A major risk to public health from the intensive approach is the high level of drug usage that is adopted by such systems and that can result in:
Another danger associated with intensive systems is the need to be continuously at the forefront of science in order to keep ahead of disease problems and attempt to increase profits. As a result, problems that previously were not experienced and expected will be encountered. The BSE crisis in the United Kingdom and, to a lesser extent, other European countries is one of the most significant examples of this. The disease appears to have developed as a result of changing the processing procedures of meat- and bonemeals in order to increase the speed of processing and reduce costs while, at the same time, using animal by-products in dairy cattle feeding in order to increase milk yields.
In this context concern also exists over the use of GMOs.
Wealthy countries generally have high per capita consumption of animal products and the poorest countries generally have the lowest consumption. For this reason, the issue of animal feed safety could be academic for many of the poorest people in the world, while the most wealthy are likely to consume only the highest-quality products, which are also likely to be the safest.
It is therefore likely that animal feed safety will become more of a problem for middle-income people who are able to buy significant amounts of animal products but only those of lower quality and lower cost; and these are likely to be of the greatest risk.
Well-informed societies have become very focused on food issues, to the point at which concern for the dangers of food safety has risen to the limits of scientific possibility. As an example, the BSE crisis in the United Kingdom has resulted in all animal products now being banned from use as animal feeds. This includes materials of pig origin, which so far have not been shown to have any link to BSE, and materials that have been approved for human consumption. At the opposite extreme, less-informed societies could become the recipients of products and technologies that are not accepted in better-informed locations. Clearly, protection should be given to the latter, to prevent them from becoming either testing grounds for new, unproved technologies or recipients of products of doubtful health status.
There is considerable variation in the regulation of the animal production and animal feed industries in different countries. While it is unlikely, and possibly inappropriate, that a common set of international standards be established, many countries are looking to develop and implement regulations that are applicable to their own circumstances. For example, the most developed countries have established very complete and in-depth sets of regularly upgraded regulations, based on many years of experience and designed to meet their own particular needs and circumstances.
It would be very useful to produce a set of general guidelines on the development and establishment of regulations, which countries could adapt to their own circumstances.
For reasons of wealth, culture and religion, many people around the world do not eat animal products. Clearly, for them this subject is irrelevant. However, since the non-consumption of animal products is often governed by lack of wealth, it is likely that such individuals could be at risk should their circumstances improve and the purchase of animal products become possible.
Within this scenario the use of by-products in the feeding of animals is likely to be the main cause of risk. This article considers the main groups of plant and animal by-product materials that offer the greatest potential risks and specifies means by which they can be used safely.
Plant by-product materials can be a potential danger to consuming animals owing to the presence of a wide range of materials including inherent toxic factors, contaminating compounds and pathogens and, possibly, genes from GMOs.
Many plants contain toxic materials or compounds that have an antinutritive effect, such as protease inhibitors, phytohaemoglutinins, gossypol, tannins, phytic acid, saponins, alkaloids, cyanogens, lathyogens, cyclopropene fatty acids, erucic acid, phyto-oestrogens, allergens, toxic amino acids (mimosine, canavanine,) antivitamin factors and anti-enzymes (Tacon, 1997). In order that plant materials can be fed to animals it is important that these compounds are bred out of plants, or removed or deactivated before consumption.
The following are some examples of toxic materials in plant by-products.
Toxic compounds. A good example of a toxic compound that is present in a well-used animal feed by-product is gossypol, which is a contaminant of cottonseed products. The use of cottonseed in animal feed has been facilitated by breeding plant types with lower levels of gossypol, removing the gossypol by physical extraction or deactivating it through the use of iron salts (Tacon, 1997; Rhee, 1993). In another case, that of erucic acid which is found in the seeds of such plants as rape or mustards, plants with low levels of the compound have been bred (Delseny, Bourgis and Roscoe, 1999).
Many other plants contain high levels of toxic elements, such as heavy metals, resulting from their cultivation on soils with a high content of these elements. This subject was reviewed by Howell (1996).
Since animals and humans have varying tolerances to toxic plant materials, it is possible for the animals that consume them to show minor or no symptoms of their presence, but human health could be damaged. For example, pigs are much more tolerant to the presence of such elements as copper, which can accumulate in their livers to levels that damage the humans who consume the affected animal products (Babnik, 1999).
Antinutritive compounds. Many plant materials contain antinutritive compounds of many types. Good examples of such products are the protease inhibitors or phytohaemoglutinins found in many leguminous plant materials (Bollini, Carnovale and Campion, 1999; Tacon, 1997).
A cooking step is sufficient to deactivate such compounds and make the materials safe to use. Without such a simple procedure, the performance of consuming animals can be greatly impaired, although there is little risk that effects will be carried on to the humans who eat the animals.
Contaminating compounds. Plant materials can become contaminated with a wide range of chemical products, which can be dangerous to the animals that consume them. Examples of such chemicals include pesticides used to control insects or plant diseases, or chemicals from poorly cleaned stores and transporting vehicles (Sechser, 1992).
While many modern pesticides are not persistent and are of little danger when used as prescribed, there is the risk that specified usage may not always be followed and that regulations vary from country to country. There is also danger in the use of those persistent pesticides that are still permitted for certain specific problems for which no non-toxic alternatives have been developed, for example, in the control of such cotton pests as bollworms (Page et al., 1999). Unless the recommended use is strictly followed, these compounds may be consumed by animals eating by-products. Some persistent pesticides can be passed on and accumulate in animals further up the food chain, as is the case with organophosphates, for example (Weis, 1997).
Plant by-products frequently contain the external coverings of the original plant products, such as skins, peals and brans. These are more likely to be contaminated than core material and, as a result, any contaminant is likely to become concentrated in by-products.
Frequently, stores and transporting vehicles are used for a wide range of materials. Plant products and related by-products can be contaminated by the residues of previously stored or transported materials, unless such practices are strictly regulated (De Luca, 1975). In addition, the surfaces of stores and many plant materials are often treated with insecticides to control storage insects (Webley, 1985; Golob, 1984).
For all of these reasons, there is probably a greater risk of plant by-products being dangerous to animal and public health than of the original unprocessed plant product.
Contaminating pathogens. The most significant risk to animal health is probably that resulting from the contamination of animal feedstuffs with pathogenic microbes or their toxins. The most important of these are the mycotoxins, which occur on many plant products and especially those of tropical origin.
Mycotoxins are secondary metabolites of fungi whose toxic effects cause a diverse range of disorders in animals and humans. In some cases they are acutely toxic and in others they are linked to certain types of cancers. The most commonly reported problems are associated with fungal contamination of grains, forages and oilseed cakes such as cottonseed and groundnut cakes. The Aspergillus spp. and Fusarium spp. of fungi, which produce several types of aflatoxins and fumonisins, respectively, are two of many well-documented examples of mycotoxins that occur predominantly on such materials in the tropics.
Reviews of the mycotoxins that are likely to occur on feeds and forages were recently produced by D'Mello and Macdonald (1997) and Scudamore and Livesey (1998), who also describe the main types and effects of mycotoxins on animal health. These authors report that recent research indicates promising prospects for the development of plant genotypes that are immune or resistant to infection by toxigenic fungi. They also state that, in the case of aflatoxin-contaminated oilseed meals, treatment with ammonia is a cost-effective method of detoxification.
Nevertheless in most situations the main approach to controlling the problem is to reduce contamination of plant products through careful field management and storage and to monitor levels of contamination on potentially contaminated materials before use.
Genes from GMOs. There is ever-increasing use of genetically modified plants and microorganisms around the world. This has been a result of the enormous potential of genetic manipulation as a way of making plants more disease- or pest-resistant. Technology also allows the nutritional composition of modified organisms to be changed and enables them to be used to produce a wide range of products such as enzymes, hormones and pharmaceuticals.
As a result of this technology, it is very likely that large quantities of by-products originating from genetically modified materials will be ingested by the world's animal and human populations and there are possible dangers to animal and human health from their use. This subject was recently reviewed by Brufau and Tacon (1999), who emphasize the necessity of exploring the safety issues of genetic modification technology fully. In particular, they draw attention to the possible direct toxicity or antinutritional effects of transgene products, the indirect or unplanned effects on gut microbial ecology and metabolism and the possibility of onward gene transfer of transgenes to the resident microflora of the gut.
The science of genetic modification is in its infancy and current assessments of risk can only be based on the limited scientific information that is available. Until there is considerably more information about the use of these products, and the longer-term implications of their use are established, there will continue to be considerable concern about the safe use of the technology in both public and scientific circles. In the meantime, regulatory agencies in countries where genetically modified products are produced or used will need to monitor and regulate their use within proven known safety standards.
The following are the main by-products from animal sources that have been focuses of concern for animal and public health:
Meat- and bonemeals. The practice of feeding rendered animal proteins to other animals has been followed throughout the world for the past 50 years. The rendering process involves the cooking of parts of animals not used in human consumption at high temperatures to make the material safe and reduce the water content to a storable level. This process is then followed by mechanical separation of tallow (fat) from the solid residue, which is then ground to form meat- and bonemeals (MBMs) (Holst et al., 2000; MAFF, 2000).
The materials used include fallen animals and all other parts of animals and poultry not used in human food which, because of the BSE problem, the United Kingdom is currently not permitting the use of in animal feeding. Instead, these materials are rendered and put into storage for later incineration; at present, 400 000 tonnes are in storage across the country. In other parts of the world, however, MBMs continue to be used in animal feeds, and the standards set throughout Europe in response to the BSE crisis are of particular interest as guidelines for others.
Research carried by the European Commission (EC) has found that the only rendering system that reduces the level of the scrapie agent - a prion held responsible for BSE and the human disease Creutzfeldt-Jakob disease (CJD) - to an undetectable amount is that of heating to a temperature of 133 ˚C at 3 bar pressure for a minimum of 20 minutes. This system has been used to set new EC standards (MAFF, 2000).
Several reports have concluded that the BSE problem first occurred in the United Kingdom because of a combination of critical factors peculiar to that country, including the existence of a sheep population in which scrapie occurs, a sheep population that is much larger than the cattle population, and a feed and cattle industry that (at the time) produced and used ruminant-derived MBM in calf rations. Many other countries feed ruminant MBM to other ruminants, but BSE did not result because of the absence of the first two critical factors.
MBM is considered a very valuable animal feed product in most parts of the world. In the preparation of this article, 94 references describing the processing, composition and use of MBM around the world over the past ten years were consulted. They describe the feeding of different MBMs to many species of domestic animal, including cattle (Enjalbert, 1996), pigs (Acurero et al., 1993), poultry (Jensen, 1990) and fish (Bureau et al., 2000). In all cases apart from that of BSE in the United Kingdom and the rest of Europe, appropriately processed MBM was shown not to have caused problems. In all circumstances, MBM performed to its compositional potential and is therefore likely to continue to be used in most of the countries where it is currently available. On the other hand, owing to the limited supply and high costs of MBM materials in developing countries, as well as the poor food conversion efficiencies obtained when they are used in ruminant feed, it is unlikely that they will be widely used in those areas.
The United Kingdom and European experience might be considered as a unique example that adds to the wider knowledge of MBM use. One lesson that might be taken from this experience is the danger of feeding animal proteins to ruminants whose digestive processes were not developed to utilize such materials.
Acid-preserved fish and carcass waste. The processing of fish and animal carcass waste with acids has been practised for many years. This subject was recently reviewed for FAO by Machin (2000), who showed that such waste materials can be preserved by using organic acids, such as formic acid, and mixtures of organic and mineral acids, such as sulphuric or hydrochloric acid. The acids preserve the materials, following comminution, through a combination of autolysis that uses enzymes from the tissues being preserved and the effect of dissociation of organic acids into cells within the mixture, thereby killing pathogens.
However, this system has not been adopted as widely as might have been expected, largely as a result of the high cost of acids and the difficulty of handling strong acids on farms in developing countries. For these reasons, the process has mostly only been applied to the preservation of fish and carcass waste for use in fur or fish farming, which are less cost-sensitive.
The alternative system for preserving such materials is to use natural fermentation to generate lactic acid. The materials to be preserved rarely contain enough suitable carbohydrate to act as a fermentative substrate, so preservation by this technique requires that a suitable fermentative substrate be added to the animal or fish material to be preserved.
Suitable fermentative substrates include easily fermented materials such as molasses or fruit wastes. Where materials rich in more complex carbohydrates are used it is often necessary to add a starter culture to initiate fermentation. Such cultures have included lactic acid bacteria such as Lactobacillus acidophilus, or L. plantarum and Streptococcus faecium. In these cases, carbohydrate sources have included maize, wheat and wheat bran, and in one situation lactic acid was produced by fermenting straw with crab and fish waste to produce a silage for feeding to cattle. The resulting silages have been fed to pigs, poultry, fish (many types), sheep, goats and poultry.
The preservation of fish and carcass waste with organic acids is dependent on the ability of the acids to dissociate across semipermeable membranes, such as cell walls, and accumulate within the cells. In the case of bacteria and other pathogenic organisms, the drop in intracellular pH kills the organism; for example, Salmonella spp., Clostridium spp. and coliforms have been killed at pHs of less than pH4.
This research has had two interesting spin-offs: the direct addition of organic acids and their salts to animal feeds in order to act as growth promoters; and the fermentation of conventional feeds so that they produce lactic acid, thus acting as growth promoters. This work has been a result of the European ban on the use of antibiotics in animal feeds and the need to identify alternative means of controlling enteric pathogenic bacteria in animal production systems.
Overall, the use of acids in the preservation of animal and fish protein wastes has been successfully applied in animal production without problems. However, were it to be applied to the destruction of BSE agents, it seems unlikely that this approach would be any more effective than rendering is. Care should therefore be taken to ensure that ruminant protein materials processed with acids are not fed back to ruminants.
In order to reduce the risk of diseases developing, acid-preserved fish and carcass waste should be fed only to monogastric animals that have already been fed this type of material and to dissimilar species.
As well as BSE-type agents, potential problems may occur when resistant parasite eggs from such nematodes as Ascaris spp. and bacterial spores are present in the materials and fed to susceptible animals. However, many of these species require an extra-animal maturation period before they can become infective and this could reduce the potential danger.
Food processing waste (swill). The waste from catering establishments, including food manufacturers and in some cases raw meat producers, is used all over the world as an animal feedstuff. Such food processing waste is often known as swill and is used predominantly in pig and, to a lesser extent, poultry feeding.
In Europe and many other developed countries the use of these materials is very firmly regulated because of the danger to animal and human health that they can cause. Currently, the EC regulations regarding this area are being modified to take account of recent knowledge associated with BSE. In the United Kingdom, because of the BSE threat, no mammalian protein is permitted to be used as animal feed, although poultry and fish wastes can be used as swill as long as they are subject to processing that meets rendering standards. The regulations also prevent the feeding of poultry waste to the same species as a means of preventing disease transmission (MAFF, 1998). In Australia, swill feeding has been prohibited in order to prevent the introduction of exotic diseases (Millan, 1999).
The regulations currently applied in the EC for swill processing involve cooking waste at 100 ºC for one hour, or at higher temperatures (up to 133 ºC) for proportionately shorter periods of time (down to 20 minutes in the case of 133 ºC at 3 bar pressure) (Heseker and Beckhausen, 1996). The regulations also require that all the facilities involved in swill processing be subject to the surveillance of veterinary authorities. Such surveillance includes regular microbiological checks, separation of uncooked from cooked materials, and inspection and approval of all the premises that receive and use such materials (MAFF, 1998). These regulations could usefully be used as guidelines for the establishment of regulations in other countries.
Problems associated with swill feeding. Some 58 references covering the past ten years and describing the processing and use of swill were consulted in the preparation of this article. One of the main topics featured in the references is the significance of disease transmission associated with swill feeding (Corso, 1997; Horst, Huirne and Dijkhuisen, 1997). In fact, swill feeding has been shown to be responsible for the transmission of such diseases as swine fever and African swine fever. In many cases, the introduction of pig diseases into countries that were previously free of them has been associated with the use of inadequately processed swill produced from airport wastes or imported human foods (Krassnig and Schuller, 1993; Smak and Galo, 1993).
Clearly, swill is a potentially very valuable animal feed raw material that would create environmental problems if not used as an animal feed. Nevertheless, it is also a potentially very dangerous product that, when not handled with care, has been shown to be a major cause of animal health breakdowns in several countries. It is therefore essential that all countries have effective processing regulations and enforcement procedures to control the handling of food processing wastes.
Faecal waste and gut contents. It is important to consider the use of poultry waste in this discussion since it is a valuable feed material in many countries, although it is not used as a feed in many developed countries because of public sensitivity about the feeding of faecal material to animals and the possible risks of disease transfer if the material is not fully processed. This subject was last reviewed by FAO in 1982.
A considerable proportion of poultry faecal waste contains undigested nutrient material as well as non-protein nitrogen (NPN) that can be utilized by ruminants in fermentative digestion. In many countries, poultry waste has been extensively used as a valuable feedstuff for all types of livestock, including poultry (Ndifon et al., 1997), although predominantly to ruminant species (Guseva, 1993). In some cases the material has been fed without any processing, and in others it has been cooked, dried and ground or ensiled with a wide range of forage materials (Onwuka, 1997).
While most references report no problems with feeding this material, some have reported disease outbreaks - including major outbreaks involving ruminants suffering from botulism (Egyed et al., 1978) - and problems when feeding faecal waste to preruminant calves arising from the hepatoxic properties of this type of material (Suttle, Angus and Field, 1981).
Faecal waste has also been fed extensively to many types of fish, including tilapias (Yousif and Alhadhrami, 1993), carp (Jayaraman, Parthasarathy and Chandrabose, 1993) and trout (Hanif, Jamil and Hammond, 1987) without problems. The fact that the fish did not appear to suffer hepatoxic problems may be because many fish actually maintain high levels of uric compounds in their blood or are able to discharge such materials with ease into the surrounding water.
Processing. From the literature, it would appear that faecal material should be heat-sterilized before being used as an animal feedstuff; although it seems likely that fermentation could be an effective process. Faecal material has been sterilized by high-temperature cooking followed by grinding (Benham and Panes, 1982). In one case, it was sterilized by heating at 133 ºC for ten hours (Mudgal, 1985). This temperature is in line with the rendering regulations applied in Europe, although ten hours would appear excessive. Material that has been ensiled also seems to have caused minimal problems. The effect of lactic acid has a sterilizing effect (Chen and Jan, 1993).
There is a need for up-to-date guidelines on safe processing and feeding of this material as both a dried heat-processed and an ensiled product. In particular, research is required, in order to confirm the effect of ensilation on the destruction of potentially pathogenic disease organisms.
Use. Because of the presence of non-protein hepatoxic materials such as uric acid it would appear logical to feed poultry faecal material to ruminant animals, which have rumen microorganisms capable of using this nutrient. Feeding to fish might have more potential than at first seems likely since any expelled NPN might act as a fertilizer to other aquatic plant species that can then become secondary feedstuffs.
Although faecal material has been fed to poultry without apparent difficulty, it would appear to have only limited benefit and some risk of disease transmission even when heat-processed.
From an environmental point of view it would seem highly beneficial to apply some form of processing to this type of material and then use it as an animal feed rather than use it for other purposes or dump it in an unprocessed form.
This article has indicated how the importance of feed safety in the management of plant and animal by-products has become much more recognized over the past few years. This has happened largely in response to the well publicized animal and human health problems that have occurred over recent years as a result of diseases associated with the use of these products.
Although the most public disease outbreaks have occurred in Europe, the potential danger is a global issue and the limited health safety infrastructures in developing countries mean that problems there could go unrecognized. There is therefore a need for all countries to be aware of the problems with animal and plant by-product processing technology, and their solutions.
The information gathered during the preparation of this article came from nearly 400 references produced over the past 20 years and from the Internet; much of this information is unavailable to many developing countries. There is a need to identify the main issues and offer an easily accessible advisory package that will permit such counties to manage their own industries.
Clearly, ensuring that materials are safe to use requires both long- and short-term approaches. In both cases, an in-depth understanding of the problems and ways to overcome them is essential. In the long term, such understanding will enable well thought out procedures for safe processing and treatment to be developed. In the short term, the feed users and regulating agencies need to understand the origins and methods of processing the materials so that monitoring systems can be established to confirm the levels and presence of any unsafe materials.
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