Amaranth in animal nutrition: A review

P G Peiretti

Institute of Sciences of Food Production, National Research Council, Grugliasco, Italy
piergiorgio.peiretti@ispa.cnr.it

Abstract

Amaranth (Amaranthus spp.) is grown extensively as a leafy vegetable and for grains for human consumption in Central America, Asia and Africa. It has also been used in many countries as a grain, forage or silage crop for many animals, including cattle, chickens, pigs and rabbits. The aim of this review is to highlight the potentialities of amaranth in animal nutrition, in order to increase the knowledge of this plant and to allow its use in animal nutrition as an alternative protein and fibre source and as a bioactive component (essential fatty acids, flavonoids, stanols, tocotrienols and squalene) source.

Key words: amaranth, digestibility, nutritive value, pig, poultry, rabbit, ruminant

Introduction

Amaranth (Amaranthus spp.) is a pseudo-cereal which has a high nutritional value, a great agronomic potential and a variety of possible uses (Ulbricht et al 2009). As reported by Venskutonis and Kraujalis (2013), this Andean crop has recently been rediscovered, due to its great adaptability to diverse environmental conditions, poor soils and a shortage of water (Barba de la Rosa et al 2009; Rezaei et al 2014). Several amaranth species are known, but only a few are utilized for human nutrition in spite of the nutritional value of the grain and its beneficial health properties (antioxidant, antitumoural, antihypercholesterolemic, etc.) (Svirskis 2003; Ulbricht et al 2009; Rivera et al 2010; Rodríguez et al 2011; Caselato-Sousa and Amaya-Farfan 2012; Amicarelli and Camaggio 2012; Alegbejo 2013). It has also been used in many countries as a grain, forage or silage crop for many animals, including cattle, chickens, pigs and rabbits (Brenner et al 2000; Pospišil et al 2009; Alegbejo 2013; Rezaei et al 2013; Seguin et al 2013; Rezaei et al 2014), but unlike its grain, amaranth forage has received significantly less research attention.

The presence of heat labile factors (tannins, saponins, lectins and trypsin inhibitors) in raw amaranth grain has led to the grain being classified as growth inhibitory and its known anti-nutritional factors limit its acceptability and utilization by poultry and other monogastrics. Moreover, the amaranth plant may contain high concentrations of nitrates, saponins, antitrypsin proteins and oxalic acid, which could represent a health risk for ruminants. Martens et al (2012), in a review on alternative plant protein sources for chickens and pigs in the tropics, reported that the lectins contained in Amaranthus cruentus are sugar-binding glycoproteins which have a potential growth inhibitory effect, while the saponins found in Amaranthus hypochondriacus may depress animal growth. Longato et al (2016) instead reported an interesting antioxidant activity and a good content of phenolic compounds in Amaranthus caudatus grain.

The aim of this review is to point out the potentialities of amaranth in animal nutrition in order to increase the knowledge of this plant and to allow its use in animal nutrition as an alternative protein and fibre source and as a bioactive component (essential fatty acids, tocotrienols, flavonoids, stanols and squalene) source.

Use of amaranth in ruminant nutrition

Amaranth has a high potential as forage for ruminants (Table 1), which have always eaten wild amaranth, and interest in amaranth as a feedstuff has recently arisen due to its high nutritive value and good fatty acid content (Peiretti et al 2018). Amaranth can be used in different ways, as a grain and as fresh, dried or ensiled forage (Chairatanayuth 1992; Yanochkin 2000; Yanochkin 2001; Rezaei et al 2009; Rodríguez et al 2011; Abbasi et al 2012), but some species of amaranth forage, due to the presence of certain anti-nutritional factors, may not be suitable as a ruminant feed (Gupta and Wagle 1988) or may require a special treatment before it can be acceptable for ruminants (Brenner et al 2000). As reported by Skultety et al (1991), cattle fed green and ensiled amaranth showed a lower level of dry matter intake than cattle fed a pelleted amaranth diet.

Amaranth is usually capable of producing high yields of very nutritious herbage (Abbasi et al 2012), and the nutritive value depends on the development stage at which the cutting is carried out (Pospišil et al 2009). Peiretti et al (2017) determined the nutritional characteristics of Amaranthus caudatus over its growth cycle, with the aim of evaluating how the development stage affects its chemical composition, in vitro digestibility and fatty acid profile, in order to determine its potential for ruminant feeding.

Several studies have shown that amaranth has superior nutritional qualities to those of common cereals and forage crops (Odwongo and Mugerwa 1980; Yue et al 1987; Pond and Lehmann 1989) and has a greater proportion of rumen undegradable protein than other common forages, such as lucerne (Sleugh et al 2001). Cervantes (1990) observed an increase in digestibility and a decrease in anti-nutrient levels when amaranth was ensiled. Rezaei et al (2009) determined the nutritive value of both fresh and ensiled Amaranthus hypochondriacus and treated with three levels of molasses (0, 5, 10% on a fresh basis). These authors suggested, on the basis of the chemical composition, mineral content, in vitro digestibility and moderate crude protein value, that this forage has a potential as a ruminant feedstuff and that amaranth can be preserved as silage when hay-making is not possible. Seguin et al (2013) studied the impact of ensiling on the nutritional quality of two Amaranthus hypochondriacus forage cultivars and characterized the oxalate content, because it is an anti-quality compound that can affect ruminant health and can lead to hypocalcemia or kidney failure, depending on its content and on the form in which it is present in the plant (usually soluble oxalate is the most hazardous form for animals). The results of their study indicated that fresh and ensiled amaranth are both highly degradable in the rumen, and that ensiling is an effective way of reducing the oxalate content (7.1-8.5 g/kg DM) in amaranth silage (Blaney et al 1982), even though the observed oxalate content of fresh amaranth (11.0-12.9 g/kg DM) was considerably lower than values that had been reported to represent health risks in ruminants (McKenzie et al 1988). Rahjerdi et al (2015) studied the potential of two Amaranthus hypochondriacus varieties, maize and an amaranth–maize combination as forage sources for ruminants, and they determined their chemical composition, silage fermentation characteristics, in situ DM degradability and in vivo digestibility in sheep. These authors reported that an improved crude protein content was obtained by mixing maize with amaranth, thus showing the potential of amaranth to complete maize in ruminant diets. Olorunnisomo and Ayodele (2009) measured the digestibility of sun-dried or ensiled maize, amaranth and maize–amaranth mixtures using West African dwarf sheep and reported that Amaranthus cruentus had the potential to produce good-quality silage. Alegbejo (2013) reported that Amaranthus retroflexus and Amaranthus hybridus have been successfully included in feeds for sheep and calves as forage, with similar results to that of lucerne. Pond and Lehmann (1989) recommended Amaranthus cruentus accession as a suitable substitute for conventional forages, such as lucerne, at levels of up to 50%, as a result of its low fibre and high crude protein contents and the absence of toxic substances in the vegetative fractions of the plant. They concluded that the studied accession had a good potential as an energy source for growing lambs, and had no effect on the weight gain or feed utilization. Odwongo and Mugerwa (1980) studied the effect of including up to 40% leaf meal of Amaranthus hybridus in early calf weaning diets, and compared the results with those obtained for dairy calves fed lucerne meal. They concluded that the calves performed well when given diets containing up to 40% amaranth leaf meal and they observed a comparable feeding value to that of lucerne meal.

As far as amaranth grain utilization in ruminant feeding is concerned, different studies have been performed. Jalč et al (1999) studied the effect of Amaranthus hypochondriacus grain used as a partial substitute (5, 10 and 20%) for barley in diets fermented in an artificial rumen and inoculated with rumen fluid and digesta from Slovak merino sheep fed a diet of 20% barley and 80% hay. The volatile fatty acids, methane, ammonia and total gas production, DM, organic matter and fibre digestibility resulted similar for all of the considered diets. Olorunnisomo (2010) determined the effects of mixing Amaranthus cruentus cultivated for fodder production with whole plant maize harvested at the dough stage, either sun-dried or ensiled, on the digestibility of the mix, and on the intake and growth of West African dwarf sheep. They found that maize fodders were better digested than amaranth fodders, or their mixture with maize, while the intake was similar for the sun-dried fodders, but higher for the ensiled maize than for the ensiled amaranth or amaranth-maize fodders. Conserved amaranth or amaranth-maize fodders determined less growth and a lower feed conversion in sheep than conserved maize fodders. Kubelková et al (2013) evaluated 10% replacement of barley by milled, mechanically ground, and ground amaranth grains (after heating in a microwave oven) in ruminant diets consisting of 70% meadow hay and 30% barley meal. They evaluated the effects of dietary inclusion of these three treated amaranth grains on the rumen fermentation and concentration of volatile fatty acids in the fermentation fluid. No detrimental changes in the in vitro fermentation parameters (concentrations of saturated or unsaturated fatty acid, production of total volatile fatty acid, fermentation gasses and pH values) were observed. These replacements only lowered the degradability of the neutral detergent fibre, but had no effect on the degradability of the acid detergent fibre or DM. The authors concluded that the addition of treated amaranth grains to ruminant diets enhanced the production of microbial protein in the effluents, and indicated that these grains could partially substitute barley.

Rezaei et al (2013) determined the effect of different dietary levels (0, 7.5, 15, 22.5 and 30%) of Amaranthus hypochondriacus silage as a substitute for maize silage on the blood chemistry parameters and carcass characteristics of fattening Moghani lambs. An amaranth silage replacement of up to 30% in the diet improved the total gain, carcass weight and carcass cuts (neck, shoulder, brisket, loin and legs), without affecting the animals’ health or the lean-to-fat ratio. No effects were recorded for the edible and non-edible offal parts or for the blood chemistry parameters, except for the triglyceride concentration, which decreased as the dietary level of amaranth silage was increased. Rezaei et al (2014) studied the effects of substituting maize silage with amaranth silage (at 0, 7.5, 15, 22.5 and 30%, respectively) on the growth performance, feed intake, in vivo digestibility, nitrogen retention, microbial protein and ruminal fermentation in fattening Moghani lambs. The average daily gain, feed intake, microbial nitrogen supply, nitrogen retention and ruminal butyrate increased as the dietary level of amaranth silage was increased, and no effects on the digestibility or feed efficiency were observed.

Use of amaranth in rabbit nutrition

Amaranth could be considered as a nutrient substitute for conventional rabbit feeds (Alfaro et al 1987; Bautista and Barrueta 2000; Molina et al 2015) and the vegetative part of the amaranth plant could be a useful resource for rabbit feeding, due to its high yield and chemical characteristics. It has been used in several experiments (Table 2) on the incorporation of forage, carbohydrate sources of energy, leaf protein and other protein concentrates in rabbit feeding (Lebas et al 2004). Reddy and Reddy (1993) reported an acceptable effect on growth, when Amaranthus hypochondriacus grain was used as a component of the rabbit rations (40%).

In order to determine the feed efficiency of amaranth on growing rabbits, Alfaro et al (1987) evaluated diets containing an increasing content (0, 15, 30, 45 and 60%) of dehydrated leaves and stalks of Amaranthus hypochondriacus, with 17.8% crude protein and 12.4% crude fibre contents to replace equal amounts of lucerne leaf meal with 22.0% crude protein and 23.3% crude fibre contents. They reported that amaranth leaf meal can efficiently replace lucerne leaf meal for up to 15% of the diet, without any negative effects on the weight gain, feed intake, feed efficiency, carcass weight or serum proteins. Higher levels of steam-treated amaranth meal (60%) in the rabbit diet caused growth retardation and a pathological picture characterized by edema and interstitial nephrosis, while a five minute steam treatment of the leaves and stalks of amaranth, prior to dehydration and milling, improved the nutritive quality of this diet. Bamikole et al (2000) determined the acceptable level of amaranth (unthreshed inflorescences or the seedheads of mature grain plants) as a substitute for oil cakes as a feed ingredient of concentrate diets for rabbits. They tested four diets: a control diet and three diets with different inclusion levels (30, 20, and 10%) and found that the weight gain and intake were reduced for the diets containing 30 and 20% of amaranth, in comparison to the diet with 10% inclusion and the control diet. The feed conversion efficiency and digestibility of the amaranth diets were higher than those of the control diet, and only minor differences were observed among the diets. The serum metabolite and haematological parameters were generally poorer for the 30% inclusion diet than for the control diet, but were better for the 20 and 10% amaranth diets. These authors concluded that unthreshed mature grain amaranth seedheads could be used as a component of the concentrate feeds of rabbits, up to a dietary level of 10%, to partially replace the expensive oil cakes in the diets. Chhay et al (2013) evaluated the foliage of amaranth as a replacement of water spinach (Ipomoea aquatica) as the basal diet (with ratios of: 0/100, 25/75, 50/50, 75/25 and 100/0) of growing rabbits. They reported negative effects on the growth rate (from 15.1 to 5.6 g/d) and DM feed conversion ratio (from 5.9 to 12.8) as amaranth foliage was used to replace water spinach as the source of forage. Furthermore, they found that a diet supplementation with paddy rice improved the growth performance, but did not compensate for the negative effects of amaranth.

Molina et al (2015) studied the effects of three experimental diets containing increasing amounts (0, 16 and 32%) of Amaranthus dubius Mart. ex Thell., which contained 39.8% of neutral detergent fibre and 20.9% of crude protein, on the performance and digestibility of growing New Zealand White rabbits. These authors reported that the health status of the rabbits was not affected by the changes in the amaranth inclusion rate, and no significant differences in weight gain or live weight were found between treatments at the end of the fattening period. The daily feed intake was higher in the rabbits fed the control diet than in the rabbits fed the supplemented diets, and the feed conversion rate improved as the amaranth inclusion level in the diet was increased. The apparent digestibility of the experimental diets showed higher values than the commercial diet, and no differences were found among the diets, except as far as ether extract digestibility was concerned. They concluded that Amaranthus dubius could be considered as an alternative source of fibre and protein for rabbit feeding in subtropical and tropical regions. Molina et al (2018) evaluated the carcass characteristics and meat quality of growing rabbits fed diets with Amaranthus dubius and reported an increase in protein and fat contents and a decrease in meat moisture with increasing level of amaranth in the diets..

As a result of its physiological effects, Amaranthus caudatus has also been used in several trials to determine the effects of its inclusion on the aortic endothelial function and lipid peroxidation in hypercholesterolemic rabbits, as a model for human consumption. Plate and Areas (2002) observed a cholesterol-lowering effect in hypercholesterolemic rabbits, when they were fed extruded defatted Amaranthus caudatus flour, in comparison to rabbits fed a control diet or a diet supplemented with amaranth oil. The rabbit groups all showed similar growth rates. They concluded that the consumption of extruded amaranth flour may be an option to prevent coronary heart diseases because it reduces (-50%) the low-density lipoprotein and total cholesterol levels in plasma. Kabiri et al (2010; 2011) studied the antioxidant effect of the aerial parts (stems, leaves and flowers) of Amaranthus caudatus and assessed the ability of its hydroalcoholic extract to regress atheromatous lesions and to reduce their new formation in hypercholesterolemic rabbits. They concluded that amaranth extract supplementation is capable of protecting cellular membranes against oxidative stress and of significantly reducing the atherogenic index and injuries of cholesterol fed atherosclerotic rabbits. Caselato-Sousa et al (2014) determined the benefits of consuming heat-expanded amaranth grain on the lipid peroxidation and aortic endothelial functions using a hypercholesterolemic rabbit model. These authors supported the notion of a lipid peroxidation process occurring as a result of high cholesterol intakes, and concluded that the intake of heat-expanded amaranth grain is able to revert an associated endothelial dysfunction, lower tissue and blood cholesterol oxidation and increment fecal cholesterol excretion in dyslipidemic rabbits.

Use of amaranth in pig nutrition

There is currently a scarcity of literature data on the use of amaranth in pig nutrition (Table 3). One sustainable approach to replacing animal-origin feeds, such as meat and bone meals, in pig nutrition is the use of amaranth and its processed products, which are able to meet the animals’ requirements (Herzig 2001), because amaranth grains have a more balanced composition of essential amino acids, a relatively high content of proteins and a good dietary fibre content, compared to conventional cereals (Písaříková et al 2005a). Moreover, it can be expected that the high content of lipids (particularly of essential fatty acids) may be effective in wholesome pork production as they modify the fatty acid composition of animal tissues (Zralý et al 2006).

As a result of the quality of amaranth protein, particularly because of the lysine content, Zralý et al (2004) studied the effect of its inclusion on the growth efficiency and selected health and metabolism parameters of pigs fed different diets containing dried surface amaranth biomass, ground amaranth grain, popped (heat-treated) amaranth grain, or meat-and-bone meal. No significant differences were detected in the growth performance of the pigs fed different diets. The biochemical parameters (total cholesterol, high and low-density lipoprotein cholesterol, albumin, total protein, triglycerides, glucose, transferases, alkaline phosphatase, magnesium, calcium and phosphorus blood plasma levels) all fell within the physiological limits, and no clinically manifested disease or mortality, related to the use of amaranth diets, was recorded. These authors, who considered that an amino acid composition with a high biological value of amaranth protein was favourable, concluded that amaranth used as both dried surface biomass and grain is a source of enough nutrients to substitute the components of animal origin in pig nutrition. Zralý et al (2006) studied the effects on the health, growth performance, carcass characteristics and meat quality of market pigs fed two different diets: the first diet contained 5% of dried surface biomass of amaranth and 5% of non-heat-treated amaranth grain and the second diet contained 5% of dried surface amaranth biomass and 5% of heat treated amaranth grain. They compared the effects on the same parameters obtained in pigs fed a diet containing 10% of lupine seed meal of a sweet cultivar or a control diet containing 3% of fish meal. The aim of this study was to find a possible substitute for animal protein that could be fed during the entire pig fattening period. They found that none of the diets adversely affected the animals’ health or metabolism, and they observed a similar average daily body weight gain, feed conversion rate, carcass characteristics and meat and sensory qualities. Sokól et al (2001) studied the effect of amaranth grain given to fatteners at a level of 25% of the diets in the different form on some slaughter evaluation indices and qualitative traits of meat. They found that this percentage of amaranth in the mixtures had no significant effect on the chemical composition, physical-chemical or sensory properties of the meat or of the carcass quality.

Shilov and Zharkovskii (2012) proposed the use of Amaranthus cruentus L. grass meal hydrolysate (in percentages of 2, 5, and 10% of mixed feed DM, respectively) as a source of vitamins and biologically active substances that would be able to promote an increase in the production and survival of weaner pigs. These authors found that the addition of 10% of this hydrolysate to the pig feed ratio increased the protein, lipid and cellulose digestibility, the degree of assimilation of nitrogen and the productivity of weaners. Kambashi et al (2014) determined the nutritive value of whole Amaranthus hybridus plants and another 19 forage plants commonly used to feed pigs in the Democratic Republic of Congo. The in vitro DM, in vitro crude protein and in vitro energy digestibilities of this plant were 0.53, 0.78 and 0.47, respectively, and these parameters were among the highest found for all the studied forage plants. Nakai (2008) studied the use of different combinations of agricultural products and natural plants in pig feeds in northern Thailand, and reported the use of a low percentage (1%) of Amaranthus mangostanus leaves and stems during the rainy season. Olufemi et al (2003) studied the effects of the inclusion of Amaranthus spinosus leaves on some blood parameters (packed cell volume, red blood cell and white blood cell counts, and haemoglobin concentration) and on the weight gain of growing pigs. They found a significant reduction in the packed cell volume, in the red blood cell counts and in haemoglobin as well as a significant increase in weight gains of the pigs administered the supplemented diet, compared to the pigs fed the control diet. These authors concluded that this leaf extract could be used in growing pig diets, but with adequate precaution to avoid any probable toxic effects, and that it could also be used as an active anthelmintic, as reported by Assiak et al (2002).

Use of amaranth in poultry nutrition

The use of unconventional sources of energy and protein, such as sun-dried leaf meal, has increased in monogastric feed formulations. Fasuyi et al (2007) showed that sun-dried Amaranthus cruentus leaf meal could be a potentially rich source of nutrients and could be added to broiler finisher diets. In fact, the anti-nutritional factors that are present in amaranth can be reduced drastically to innocuous levels as the result of the processing effect of sun-drying. The most suitable inclusion level of Amaranthus cruentus leaf meal to obtain a better performance in broiler finisher birds, without any adverse effects, was found to be 10%. Fasuyi and Akindahunsi (2009) found that sun-dried Amaranthus cruentus leaf meal can only be included in broiler diets in percentages of up to 25%, when supplemented with an enzyme (cellulase, glucanase and xylanase) cocktail.

Grain amaranth, which has about twice the amount of protein as cereal grains, a superior amino acid composition and similar energy content, can be used as a feed ingredient for broilers, and it should only be included as raw material in finisher diets (Table 4). In fact, a heat treatment, in the form of autoclaving, extrusion, atmospheric cooking, toasting or popping, is usually necessary to partially or completely destroy its growth depressing factors for growing chickens. Nevertheless, Písaříková et al (2005b) showed a higher in vitro digestibility of protein in raw amaranth than in popped grain, and they related this to the decreased biological value of protein that occurs at high temperatures. Other authors have instead reported the same or an increased nutritional value of amaranth grain after a heat treatment, a result that can be explained by considering the limiting effect of heat-labile anti-nutritive compounds (Bressani et al 1987).

The steam pelleting of diets containing amaranth grain has usually led to increased feed intake and growth performances, with a higher fat deposition in broilers. Tillman and Waldroup (1986) suggested a maximum inclusion level of 40% for Amaranthus cruentus grain in broiler diets, but only when the amaranth is properly processed by either extrusion or by autoclaving. These authors also found similar body weight gains in the chickens fed the control diet and in the chickens fed grain amaranth autoclaved for 60 min or extruded “normal” or “dry”. Tillman and Waldroup (1988a, 1988b) showed that extruded grain amaranth can be fed to broiler chickens without any adverse effects, and they determined the apparent metabolizable energy and apparent amino acid availability values of extruded grain amaranth. Tillman and Waldroup (1988c) determined the effects of feeding maize-soy rations supplemented with 0, 10, 20, 30, 40, or 50% of amaranth extruded grain on the performance of male broilers. Each diet was formulated to meet the nutrient requirements of the starter, grower and finisher periods. No differences were found for the feed utilization or dressing percentages, but the birds fed the control diet weighed significantly more and had significantly higher dressed carcass weights than those fed the 50% amaranth diet. Acar et al (1988) determined the nutritional value of different raw and autoclaved amaranth products (whole flour, fat-free flour, perisperm and bran) and popped amaranth in growing chickens, and concluded that autoclaved amaranth grain and its perisperm fraction gave comparable production results to those of chickens fed a control diet composed primarily of maize and soybean meal and containing about the same apparent metabolizable energy and crude protein levels, while the feeding of popped amaranth resulted in a poorer performance. Ravindran et al (1996) compared the feeding and energy utilization values of raw Amaranthus hypochondriacus incorporated at 0, 20, 40 and 60% levels into a broiler diet based on maize + soyabean meal + meat meal, and they found that increasing levels of raw amaranth in the diet depressed the feed intake and weight gains. However, the growth-depressing effect of raw amaranth grain was overcome by autoclaving; in fact, chicks fed on 20 and 40% autoclaved amaranth diets presented similar weight gains, feed intakes and feed/gain ratios to those fed the control diet. These authors showed that autoclaved grain amaranth (130°C for 1 h) is a potentially useful energy supplement with an improved apparent metabolizable energy and that it can be incorporated at levels of up to 40% without any adverse effects on performance.

Waldroup et al (1985), Serratos (1996), Rouckova et al (2004), and Písaříková et al (2006) reported no differences in the live weight of broiler chickens fed both untreated and heat treated amaranth diets, compared to the control diets. Waldroup et al (1985) showed that Amaranthus hypochondriacus and Amaranthus cruentus grain may be utilized by broiler chickens, and they found that 20% of raw and autoclaved grain could be incorporated in broiler diets. The feed intake was reduced slightly for this inclusion level, while the weight gain of the chickens fed the amaranth diets did not differ significantly from that of the chickens fed the control diet, which was based on maize-soybean meal. Chickens fed diets containing 40% of raw or autoclaved amaranth showed a significant reduction in weight gains and feed intake, although the performance reduction was partially alleviated by autoclaving, and it was more severe in chickens fed Amaranthus hypochondriacus grain. Rouckova et al (2004) evaluated the possibility of substituting a component of animal origin (meat-and-bone meals) included in vegetable diets for broilers with 7% of amaranth grain with or without a heat treatment. They investigated the effect of this substitution on the performance and selected biochemical parameters (concentrations of proteins, glucose, cholesterol and total lipids in the blood sera). No statistical differences in the live weights were found at the end of the experiment between the chickens fed the amaranth diet and the chickens fed the diet including meat-and-bone meals. These authors concluded that amaranth could be successfully used as a substitute for meat-and-bone meals in broiler chicken diets, as the inclusion of heat-treated amaranth had no effect on the protein concentrations, compared to the control group, whose diet included a component of animal origin, and because the glucose level was significantly lower in the chickens fed amaranth than in the chickens fed a mixture containing meals of animal origin, while the total lipids and cholesterol levels were higher. Písaříková et al (2006) studied the effects of various forms of amaranth (crude grain, heat processed grain, dried above-ground biomass), used as a replacement of animal protein (fish meal), on the live weight, feed conversion, carcass characteristics and meat quality of broiler chickens, and observed no negative effects of the diets with amaranth.

Kabuage et al (2002) studied the effect of eight different diets, with 20 or 40% inclusion levels of Amaranthus hypochondriacus grain, with or without molasses, on the performance, carcass composition and histopathology of the pancreas and liver of broiler chickens. Four diets were steam pelleted at 70°C, while the other four were administered in mash form. The diets were all compared with a maize-soybean meal control diet. The pelleting of the amaranth in the diets was beneficial in improving the body weight, feed intake, feed efficiency and carcass fat in 8 week-old broiler chicks, while the inclusion of molasses did not increase the growth performances. These authors reported only a moderate change in the histopathology of the liver and pancreas that could not be attributed to the feeding of amaranth. Písaříková et al (2005b) determined the apparent digestibility of broiler chickens fed experimental diets containing 10% of raw and 10% of popped amaranth, compared to a cereal feed mixture without amaranth. They concluded that raw grain induced a high apparent digestibility coefficient, a high crude protein content and a favourable fibre and amino acid composition; therefore, raw amaranth grain could be a suitable supplement in feed mixtures for broiler chickens at 10%.

The squalene and tocotrienol compounds contained in amaranth varieties could affect the cholesterol biosynthesis of poultry. Qureshi et al (1996) studied the effect of dietary supplementation of amaranth ( Amaranthus hypochondriacus and Amaranthus cruentus) and its oil on the cholesterogenesis of chickens. They found that birds fed amaranth diets showed a 10 to 30% decrease in total cholesterol and a 7 to 70% decrease in low-density lipoprotein cholesterol, compared to chickens fed a control diet, while the high-density lipoprotein cholesterol values remained unchanged in all the groups. They observed that the activity of the enzyme that is responsible for the breakdown of cholesterol (cholesterol 7 alpha-hydroxylase) was 10% to 18% lower in the control group than in the experimental group, and they stated that the inhibition of the rate-limiting enzyme for cholesterol biosynthesis (liver 3-hydroxy-3-methylglutaryl coenzyme A reductase), with a reduction of 9% in the liver of birds fed amaranth and its oil, was not only due to the presence of squalene and tocotrienols, but also to the presence of other potent cholesterol synthesis inhibitors in the amaranth diets.

Longato et al (2017) evaluated the growth performance, blood serum metabolites, oxidative status, and meat quality of broilers fed diets containing 0, 5 and 10% of Amaranthus caudatus grain, respectively. They reported no differences in the alanine aminotransferase and albumin levels or in the meat quality characteristics, while the serum antioxidant power was significantly higher and the growth performance, cholesterol, triglyceride and serum lipid peroxidation levels were significantly lower in the broilers fed diets supplemented with 5 and 10% of amaranth, compared to the broilers given a diet without supplementation.

Króliczewska et al (2008) studied the influence of 0, 2, 5 and 10 % supplementation of Amaranthus cruentus grain on the biochemical and haematological blood parameter values of laying hens. The increase in inclusion level of amaranth did not affect the erythrocytes, leukocytes, hematocrit, haemoglobin or iron content. A beneficial effect of the supplemented diets on the lipid parameters of the blood (with a decrease in the low-density lipoprotein cholesterol and triglycerides) and changes in the activity of aspartate aminotransferase and alanine aminotransferase were observed, compared with an un-supplemented group.

Popiela et al (2013) determined the performance, blood characteristics, egg traits and egg yolk fatty acids composition in Lohmann Brown laying hens fed diets containing 0, 5 and 10% of extruded amaranth grains. The hens fed diets with 5% of amaranth showed the lowest feed conversion ratio and the greatest egg production. The health conditions were not affected by the supplementation of extruded amaranth grains, as concluded from an observation of the good values of the blood characteristics (hematocrit, haemoglobin, iron, glucose, aspartate aminotransferase alanine aminotransferase, total protein, albumin, total cholesterol, HDL-cholesterol and triglycerides), while the glucose, aspartate aminotransferase and alanine aminotransferase decreased as the extruded amaranth grain supplementation was increased. Egg quality (measured as Haugh units) and other parameters, such as breaking strength of the egg shells, thick albumen height, egg and shell weight, albumen and yolk weight, fatty acid content of the egg yolk, did not differ among the hens fed different diets. The results of a sensory analysis of the eggs were similar between the supplemented and control diets. Punita and Chaturvedi (2000) fed Amaranthus paniculatus grain and red palm oil, which is known to be a hypocholesteromic agent, to laying hens to reduce the cholesterol content of the eggs by means of diet manipulation. These authors determined the cholesterol, total lipids and PUFA contents in the experimental and control eggs, and found an increase in the linoleic acid content of about 100 % and a reduction in the cholesterol content of the eggs in the experimental groups of 14 %. The maximum reduction in cholesterol and in the total lipid content was observed in the eggs of the hens fed red palm oil and red palm oil + popped amaranth, while significant increases in linoleic acid content were found in the eggs from the red palm oil + popped amaranth, red palm oil and raw amaranth groups. They concluded, on the basis of the results of a consumer test, that these lower cholesterol eggs were well accepted. The effect of amaranth addition to laying hen fodder on the egg yolk lipid fractions was also studied by Bartkowiak et al (2007). They compared four inclusion levels of amaranth grains (0, 2, 5 and 10%) in diets and determined the cholesterol, vitamin A and fatty acid contents in the egg yolk. No statistically significant differences were reported between groups. Reklewska et al (1995) determined egg quality using amaranth in laying hens, and quantified the level of triacylglycerides and the saturated fatty acid content in the hens’ egg yolk. Vishtakalyuk et al (2001) investigated the potential applications of amaranth vitamin-herbal flour, obtained from Amaranthus cruentus, to feed egg-laying hens of different age groups. This herbal flour positively influenced egg laying and the egg mass, in comparison to lucerne or cereal flour, because amaranth has a high nutrient value, low toxicity and a positive effect on the productivity and physiological state of hens of all age groups. This was correlated to the high content of essential amino acids in amaranth, as well as the unique lipid, mineral and vitamin composition of amaranth. These authors found an increase in egg laying of 9.2%, when amaranth vitamin-herbal flour was added at 3% to the hens’ ration; moreover, the quality of incubated eggs was improved, and the growth of younger hens was facilitated. A deterioration in the physical state of the birds was noted when the hens were fed 16-18% of amaranth phytomass, probably due to the presence of anti-nutritional factors in the amaranth, or to an excessive level of cellulose or some amino acids in the ration. Tillman and Waldroup (1987) incorporated 0, 10, 20 or 30% of extruded Amaranthus cruentus grain into soybean-maize meal rations for Comb White Leghorn laying hens, without detrimentally altering the production characteristics of the eggs. No differences were observed for the shell thickness, shell strength, egg quality (measured as Haugh units) or number or severity of blood spots. The yolk colour decreased as the amaranth inclusion level was increased, and the authors suggested adding pigment to the amaranth diets to improve the yolk colour. Moreover, the hens fed the control diet required significantly larger feeds to produce a gram of egg or a dozen eggs than those fed the diets containing amaranth. The egg weights were higher and the egg production was lower for the hens fed the control diet than for those fed diets containing 10 and 20% of amaranth.

Conclusions

• This review describes the different uses of amaranth in animal nutrition as an alternative protein and fibre source and as a bioactive component source.
  
  
• Amaranth is mainly used as fodder to feed ruminants and rabbits, while grains submitted to a heat treatment in order to reduce the effects of anti-nutritional factors are mainly used for monogastrics.
  
  
• Among the beneficial health properties that can be obtained, amaranth showed an interesting cholesterol-lowering effect in animals fed this plant. Thus, amaranth could be used to reduce the cholesterol content in products of animal origin.

Acknowledgments

The author would like to thank Mrs M. Jones for the linguistic revision of the manuscript.

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Received 1 February 2018; Accepted 10 April 2018; Published 1 May 2018

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