Purified lignin: Nutritional and health impacts on farm animals—A review

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Animal Feed Science and Technology 144 (2008) 175–184

Review

Purified lignin: Nutritional and health impacts on farm animals—A review B. Baurhoo a , C.A. Ruiz-Feria b , X. Zhao a,∗ a

Department of Animal Science, McGill University, Ste Anne de Bellevue, Quebec H9X 3V9, Canada b Department of Poultry Science, Texas A&M University, College Station, TX 77843-2472, USA

Received 10 July 2007; received in revised form 20 October 2007; accepted 25 October 2007

Abstract Lignin, the second most abundant natural compound after cellulose (Boudet and Grima-Pettenati, 1996), is a high-molecular weight polymer of phenolic compounds that occurs naturally in plants. It is mostly present in the cell wall, conferring structural support, impermeability and resistance to microbial attack. Commercial purified lignin is produced as a by-product of the paper industry, separated from wood by chemical pulping processes. These purified lignins are low molecular weight mono-phenolic fragments that have biological characteristics that differ from those of native lignin. Different chemical treatments during wood-pulping processes yield diverse types of purified lignin, such as Alcell lignin and Kraft lignin. Although these phenolic fragments may potentially have important applications in animal agriculture, research with purified lignin has not received much attention and there are few published results. In contrast to native lignin, purified lignin does not represent a barrier to digestion in monogastric or ruminant animals. Several in vitro and in vivo studies have demonstrated antimicrobial properties of the phenolic fragments in purified lignin. Recently, purified Alcell lignin has been shown to exhibit prebiotic effects in chickens, favouring growth of beneficial bacteria and improving the morphological structures of the intestines, as measured by increased villi height and goblet cell number. These findings suggest that purified lignin may exert health benefits in monogastric animals and could potentially be considered as a natural feed additive. Based on the few published studies, animal responses to purified lignin seem dependent on dosage, animal species and type and source of the lignin product. More research

∗

Corresponding author. Tel.: +1 514 398 7975; fax: +1 514 398 7964. E-mail address: [email protected] (X. Zhao).

0377-8401/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.anifeedsci.2007.10.016

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is required before establishing conclusive benefits of purified lignin on animal performance and health. © 2007 Elsevier B.V. All rights reserved. Keywords: Lignin; Intestinal health; Antibiotics; Livestock

Contents 1. 2. 3.

4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Origin and chemical structure. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Purified lignin and animal performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Antimicrobial properties of purified lignin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. In vitro studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. In vivo studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Prebiotic effects of purified lignin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

176 177 179 179 180 180 182 182 182

1. Introduction Lignin refers to a group of phenolic polymers that confer strength and rigidity to the woody cell wall of plants. It is the second most abundant natural compound after cellulose on earth (Boudet and Grima-Pettenati, 1996) and represents up to one-third of plant cell walls (Pan et al., 2006). Research on naturally occurring poly-phenols has received more attention in human medicine, versus animal agriculture, as poly-phenols exert several health benefits in humans. First, they inhibit oxidation of low-density lipo-proteins, thereby decreasing risks of heart disease (Meyer et al., 1997; Heinonen et al., 1998). Second, poly-phenols possess anti-inflammatory and anti-carcinogenic properties (Shahidi and Wanasundara, 1992; Miyake et al., 1999; Wang et al., 1999) and third, they are effective antioxidants for food lipids (Shahidi and Wanasundara, 1992). Indeed, the phenolic fragments of Kraft lignin, obtained as a by-product during cellulose extraction in the paper manufacturing process by alkaline hydrolysis of wood, is as effective as vitamin E as an antioxidant in humans (Catignani and Carter, 1982). In animal agriculture, however, native lignin is mostly regarded as a barrier to nutrient digestibility. Presumably for this reason, purified lignin has not received much scientific interest and its potential as a feed additive is not well recognized. To feed manufacturers, lignin, as lignosulphonate, is a useful feed pellet binder. However, until recently, there has been no interest in lignin as a biological feed additive in animal nutrition. The link between use of growth promoting antibiotics and antibiotic-resistance of pathogenic bacteria in humans has led member countries of the European Union to ban use of these antibiotics in animal agriculture. At the same time, recent findings demonstrate that purified lignin encompasses production and health benefits in animals in the absence of antibiotics. For this reason, purified lignin is one of several natural compounds that have received new

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interest and scientific consideration as a natural feed additive. Purified lignin may potentially mitigate production and economic losses after the use of antibiotics in livestock production is discontinued. In its purified form, lignin contains several low molecular weight phenolic monomers that possess biological effects not characteristic of native lignin. So far, much emphasis has been put on production and health benefits of phenolic monomers, such as carvacrol and cinnemaldehyde (Lee et al., 2004; Bozin et al., 2006), in farm animals, but less has been done with purified lignin that contains several mono-phenolic fragments. The possibility exists that mono-phenolic fragments of purified lignin may have beneficial effects on productivity of farm animals, safety of animal products and the environment. This paper reviews data on nutritional implications of purified lignin on productivity and health in farm animals.

2. Origin and chemical structure Lignin is a complex poly-phenolic, high-molecular weight polymer, naturally occurring in the cell walls of plants and trees. It is essential as mechanical support to leaf blades and stems, and imparts strength and rigidity to plant walls. In plants, lignin also acts as an inducible physical barrier against pests and diseases (Vance et al., 1980). As physiological maturity of a plant advances, its lignin and phenolic acid contents increase (Morrison, 1980; Theander et al., 1981). Other factors, such as temperature, light intensity, water availability, latitude, harvest and storage periods also affect lignin contents of plant materials (Van Soest, 1994, 1996). Polymerization of low molecular weight phenolics occurs during drying of plant materials. It is known that lignin content also varies among plant species. For example, legume fiber is more lignified than grasses, but legumes are typically more digestible because they contain less fiber, their fiber is more rapidly digested, and lignin is concentrated mostly in the stems leaving the leaf fiber relatively lignin-free. Lignin is thought to interfere with microbial degradation of fiber polysaccharides by acting as a physical barrier, and by cross-linkages to polysaccharides by ferulate bridges. Several grass cell types become lignified during maturation, whereas xylem and tracheary cells are the only major lignified tissues in legumes (Wilson, 1993). Native wood lignin (Fig. 1), contains 11 phenolic monomeric fragments (Zemek et al., 1979), with coumaric and ferulic acids being the primary phenolics in forages. Lignin is synthesized by an enzyme which initiates dehydrogenative polymerization of three monomeric aromatic alcohols ␳-coumaryl, coniferyl and synapyl alcohols (Jung and Fahey, 1983; Boudet and Grima-Pettenati, 1996). Variation in lignin concentrations among plant species is due to differences in the proportions of these alcohols. For example, Jung and Fahey (1983) reported that softwood lignin contains about 800 g/kg coniferyl, 140 g/kg ␳-coumaryl and 60 g/kg synapyl, whereas lignin from hardwoods consists of 560 g/kg coniferyl, 40 g/kg ␳-coumaryl and 400 g/kg synapyl alcohols. The strong carbon–carbon and ether linkages in lignin make it resistant to degradation. For this reason, lignin is generally accepted as the primary entity responsible for limiting digestion of forages, thereby reducing its nutritional value (Besle et al., 1994; Van Soest,

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Fig. 1. Phenolic monomeric fragments of wood lignina,b . a 1: Eugenol; 2: isoeugenol; 3: syringaldehyde; 4: coniferylalcohol; 5: ferulic acid; 6: 4-hydroxy-3-methoxy-␤hydroxy-propiophenone; 7: 1-(4-hydroxy-3-methoxyphenyl)-2-propanone; 8: 2-(4-hydroxy-3-methoxyphenyl)-7methoxy-3-methyl-5-propyl-coumaran (“dehydro-diisoeugenol”); 9: pinoresinoldione (“dehydrodiferulic acid”); 10: Di-O-acetylpinoresinol; and 11: 2,3-bis(␣-hydroxy-vanillyl)-1,4-butane-diol b Zemek et al. (1979).

1994). Lignin is not digested by monogastric animals, but the rumen bacterial flora facilitates degradation of benzyl ether linkages of lignin polymers (Kajikawa et al., 2000). In wood, lignin is strongly intermeshed with cellulose and hemicellulose by noncovalent forces or covalent bonds to form carbohydrate complexes (Perez et al., 2002), and does not exist in a pure form (Lawoko et al., 2005). In the paper-making industry, purified lignin is recovered as a by-product of cellulose production during wood-pulping. However, differences in pulping treatments yield different lignin fragments. In the sulfite process, sulphuric acid is used to convert lignin into lignosulphonates. The Kraft

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process, which uses sodium hydroxide and sodium sulphide to extract lignin from cellulose in the wood fibers, is more efficient and yields stronger fiber. In contrast, the Alcell process disrupts the chemical integrity of native lignin, thereby yielding purified lignin fragments as a co-product (Pye, 1996). This process involves aqueous ethanol as the cooking liquor at temperatures between 185 and 195 ◦ C. In contrast to Kraft and sulphite lignin, Alcell lignin consists of low molecular weight phenolic fragments with enhanced hydrophobicity (Lora et al., 1993). Hence, lignin, in its purified form, possesses chemical structures that differ from native lignin. For this reason, purified lignin may possess biological properties not characteristic of native lignin. Purified lignin is mostly used for industrial and construction purposes, and has no known application in animal agriculture.

3. Purified lignin and animal performance Reports on effects of lignin on animal performance are limited, and lignin has not been reported as a feed additive in livestock production. However, recent studies revealed positive effects of purified lignin on animal performance. Alcell lignin (12.5 g/kg of DM) improved body weight gain of Holstein calves (Phillip et al., 2000); but, no benefit was observed at higher dietary lignin levels (i.e., 25 or 50 g/kg). Indulin (40 and 80 g/kg of DM), a purified Kraft lignin from the paper industry, improved weight gain and feed efficiency in broiler chickens (Ricke et al., 1982). In geese, supplementation of a purified lignin from plant fiber improved daily weight gain, but feed was utilized less efficiently (Yu et al., 1998). The authors attributed this effect to a more rapid rate of digesta passage through the gastrointestinal tract. Alcell lignin (12.5 g/kg of DM) affected neither body weight nor feed efficiency in pigs (Valencia and Chavez, 1997). Similarly, in the absence of growth promoting antibiotics, Alcell lignin (12.5 or 25 g/kg of DM) neither altered body weight nor feed efficiency in broiler chickens (Baurhoo et al., 2007a,b). These findings suggest that differences in the forms and concentration of lignin, as well as animal species, may contribute to variable animal responses. 3.1. Antimicrobial properties of purified lignin The antimicrobial properties of the phenolic fragments of lignin are well recognized. The natural durability of many wood species is related to the potential toxicity to micro-organisms of phenolics deposited in the process of heartwood formation. Phenolic compounds have long been used as food preservatives to inhibit microbial growth (Davidson and Branen, 1981) with phenolic acids and flavonoids being the two main groups of such preservatives. Moreover, phenolic monomers, such as carvacrol and cinnemaldehyde, have been shown to be effective in fresh fruits and vegetables, rice, cheese and meat (Smid et al., 1996; Ultee et al., 2000; Skandamis and Nychas, 2001; Smith-Palmer et al., 2001; Roller and Seedhar, 2002). There is potential that purified lignin may improve intestinal health and animal welfare, but this application has not received much scientific consideration.

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Table 1 Antimicrobial effects of lignin fragments (minimal inhibitory concentration, ␮g/ml)a Compoundb

Escherichia coli

Saccharomyces cerevisiae

Candida albicans

Bacillus licheniformis

Micrococcus luteus

Aspergilus niger

1 2 3 4 5 6 7 8 9 10 11

3000 100 375 375 375 375 375 180 150 150 375

3000 100 375 1400 187 375 375 90 150 150 375

3000 100 375 2800 375 375 375 180 150 150 375

250 50 177 375 375 187 375 90 150 150 375

250 50 177 375 375 187 375 90 150 150 375

3000 250 700 3000 700 750 750 640 600 600 750

a

Zemek et al. (1979). 1: Eugenol; 2: isoeugenol; 3: syringaldehyde; 4: coniferylalcohol; 5: ferulic acid; 6: 4-hydroxy-3-methoxy-␤hydroxy-propiophenone; 7: 1-(4-hydroxy-3-methoxyphenyl)-2-propanone; 8: 2-(4-hydroxy-3-methoxyphenyl)-7methoxy-3-methyl-5-propyl-coumaran (“dehydro-diisoeugenol”); 9: pinoresinoldione (“dehydrodiferulic acid”); 10: Di-O-acetylpinoresinol; and 11: 2,3-Bis(␣-hydroxy-vanillyl)-1,4-butane-diol. b

3.2. In vitro studies The phenolic components of lignin have been reported to inhibit growth of microorganisms such as Escherichia coli, Saccharomyces cerevisiae, Bacillus licheniformis and Aspergillus niger (Zemek et al., 1979). However, the minimum inhibitory concentrations demonstrate variability in the antimicrobial activity of different phenolic fragments (Table 1). The side chain structure and nature of the functional groups of the phenolic compounds are major determinants of the antimicrobial effects of lignin. In general, phenolic fragments with functional groups containing oxygen (–OH, –CO, –COOH) in the side chain are less inhibitory, whereas isoeugenol has been reported to be the most inhibitory phenolic fragment due to a double bond in the ␣, ␤ position of the side chain, and a methyl group in the ␥ position (Fig. 1). Ferulic acid has been reported to inhibit growth of Saccharomyces cerevisiae at a concentration of 2.5 mM (De Greef and Van Sumere, 1966). The poly-phenolic fragments of Alcell lignin (100 g/l) reduced growth of Escherichia coli, Staphylococcus aureus and Pseudomonas in liquid culture (Nelson et al., 1994). It has been reported that the antibacterial effect of lignin is dose related, with more inhibition of E. coli in culture media containing 100 g/l versus 50 g/l of Alcell lignin (Phillip et al., 2000). 3.3. In vivo studies Indulin (40 and 100 g/kg of DM) reduced VFA concentrations in the ceca and large intestine of chickens (Ricke et al., 1982), suggesting that purified lignin altered the fermentation pattern of the chicken intestinal tract by inhibiting growth of certain bacteria. In a mouse model, Alcell lignin did not alter aerobic bacterial growth in the cecum, but reduced translocation of these bacteria in the lymph nodes and liver after burn injury (Nelson et

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al., 1994). In mice, a pine wood lignin was reported to possess antitumor (Sakagami et al., 1991) and antibacterial properties against the pathogens Escherichia coli and Pseudomonas (Oh-Hara et al., 1990). Ruminant responses to dietary lignin are variable. Alcell lignin had no effect on rumen fermentation in sheep, and did not alter fecal concentrations of anaerobic, aerobic and coliform micro-organisms in calves (Phillip et al., 2000). This could be the result of degradation of the phenolic compounds of lignin by rumen microbes (Kajikawa et al., 2000). Para-coumaric and ferulic acids are extensively converted into reduced phenolics by ruminal micro-organisms, as evidenced by their high ruminal disappearances (Chesson et al., 1982; Bourquin et al., 1990). Martin (1982) demonstrated that infusion of phenolic compounds, such as quinic acid, phenolic benzoic and phenylacetic acids, into the sheep rumen caused large increments in urinary outputs of phenolic acids and phenols. These observations suggest that phenolic monomers are extensively metabolized by the rumen microbial flora to more chemically reduced forms, which are subsequently absorbed and metabolized. It seems, therefore, that the antimicrobial action of lignin may be species dependent, and occurs mostly in nonruminants. In an attempt to provide a better evaluation of the antibacterial effects of lignin, Baurhoo et al. (2007b) orally challenged broiler chickens with pathogenic strains of Escherichia coli (serotypes O2 and O88) and fed antibiotic-free diets, or one containing Alcell lignin or antibiotics. Alcell lignin reduced cecal concentrations of total Escherichia coli after 3 and 9 days. Escherichia coli inhibition was more pronounced at higher concentrations (25 versus 12.5 g/kg of DM), suggesting that the antibacterial effects of Alcell lignin mostly occurs at higher doses. Further research demonstrated that dietary Alcell lignin reduced concentrations of Escherichia coli in poultry litter when compared to antibiotic-free diets or one containing antibiotics (Baurhoo et al., 2007a). Intestinal Escherichia coli contaminates poultry carcasses during slaughter (Heyndrickx et al., 2002), thereby representing an important cause of food-borne illnesses in humans. At the same time, poultry litter may contribute to the spread of antibiotic resistant genes into the food chain (Nandi et al., 2004). Moreover, litter Escherichia coli is the major causative pathogen implicated in cellulitis, a major cause of carcass condemnation at processing plants (Kumor et al., 1998). These findings suggest that purified Alcell lignin may represent a dietary strategy to reduce Escherichia coli load in the chicken intestine and litter that could offer an opportunity to improve the safety of poultry products and the control of cellulitis. Effects of purified lignin on these variables remains to be studied. The exact mechanism underlying lignin action is not well defined. In a review, Jung and Fahey (1983) suggested that the poly-phenolic compounds of lignin cause cell membrane damage and lysis of bacteria with subsequent release of cell contents. Mono-phenolic compounds, such as carvacrol, thymol and cinnamaldehyde, also possess anti-bacterial properties (Lee et al., 2004; Bozin et al., 2006). Carvacrol and thymol exhibit antimicrobial effects by causing bacterial cell membrane disintegration and release of cell contents (Helander et al., 1998). In contrast, cinnamaldehyde penetrates the bacterial cell membrane to reduce intracellular pH and cause ATP depletion (Oussalah et al., 2006). The antibacterial mechanistic actions seem to vary among phenolic compounds. Up-to-date, there is

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no report that establishes the mode of action of a product consisting of multiple phenolic compounds. 3.4. Prebiotic effects of purified lignin Prebiotics are indigestible feed ingredients which selectively stimulate growth or metabolic activity of a limited number of intestinal micro-organisms in birds and mammals (Gibson and Roberfroid, 1995). Lactobacilli and Bifidobacteria are beneficial bacteria that limit intestinal colonization of pathogens by competing for nutrients and binding sites (Rolfe, 2000), and by secreting anti-bacterial substances (Gibson and Wang, 1994; Jin et al., 1996a,b). We found that Alcell lignin (12.5 g/kg of DM) increased intestinal concentrations of Lactobacilli and Bifidobacteria in broilers (Baurhoo et al., 2007a,b). However, at higher level (i.e. 25 g/kg of DM), lignin inhibited growth of these bacteria. The strong bactericidal properties of high lignin levels have previously been demonstrated in both in vitro and in vivo studies. Prebiotics may also play important roles in improving the intestinal morphology of animal species. Longer villi are generally correlated with better intestinal health and improved efficiency of digestion and absorption. Goblet cells are responsible for the production of mucins which destroy intestinal pathogens (Blomberg et al., 1993). In broiler chickens, Alcell lignin (12.5 g/kg of DM) increased villi height and goblet cell number (Baurhoo et al., 2007a). However, there was no benefit at a higher lignin level (i.e. 25 g/kg of DM), suggesting that the prebiotic effect of Alcell lignin only occurs within a limited inclusion range.

4. Conclusions Purified lignin has biological effects other than those of native lignin. Purified lignin, such as Alcell lignin, exhibits prebiotic effects in monogastric animals by favouring growth of beneficial bacteria and improving morphological structures in the intestines. Additionally, the bactericidal properties of lignin fragments may help in the control of intestinal pathogens, thereby ensuring safety of livestock products to humans. However, much research is still required to determine optimum lignin dosage, associated health and production benefits, welfare, and safety of animal products in different livestock species, as well as potential effects on the environment.

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