Physiology of lipid digestion and absorption in poultry

1 | INTRODUCTION

Due to the impact of climatic changes and other global events such as conflict, the Covid‐19 pandemic, recession, and supply chain issues, conventional feed ingredient prices are continually increasing. The effect of these constraints is felt largely in developing countries that are coming under huge pressure to source raw materials such as corn and soybean meal (Abro et al., 2020). The search for alternative feed ingredients to sustain the livestock industry is therefore imperative. The addition of dietary oil and fat in poultry diets has been greatly overlooked as a substantial energy source (Ravindran et al., 2016). In addition to a higher energy density that is almost twice the same amount of carbohydrates and protein, dietary fats and oils are relatively inexpensive as compared to corn. Therefore, the use of dietary lipids provides a plausible alternative at increasing the energy density of diets for the high‐performing modern broiler at relatively lowered costs (Ahmadi‐Sefat et al., 2022).

Other than raising the caloric level of a diet, lipids increase the efficiency of utilising consumed energy, supply essential fatty acids and fat‐soluble vitamins (A, D, E and K), reduce dustiness, improve the integration of mash diets and slow down the rate of feed passage in the gut, allowing more time for improved nutrient digestion and absorption (Ravindran et al., 2016; Valaja & Siljander‐Rasi, 2001). Figure 1 summarises the nutritional, biochemical, and physiological roles of dietary lipids in animals. However, there is a physiological age‐related depression in the capacity of young birds to utilise dietary lipids effectively (Oketch et al., 2022). Therefore, several strategies toward optimising the energy‐yielding potential of dietary lipids including the supplementation of exogenous emulsifiers have been investigated (Ravindran et al., 2016).

For optimal digestion and absorption of dietary lipids, emulsification, lipolysis and micelle formation should occur effectively. The use of dietary exogenous emulsifiers amplifies the natural emulsifying process that is innately undertaken by taurine‐conjugated bile salts and monoglycerides. Emulsifiers are known to increase the active surface area of lipase to breakdown large fat globules into smaller fat droplets, thus aiding the absorption process of dietary lipids (Ko et al., 2023). In recent years, the addition of emulsifiers into broiler diets has become commonplace. Some of the emulsifiers tested in broiler diets are sodium stearoyl‐2‐lactylate, glycerol polyethylene glycol ricinoleate (PEGR), lysolecithin, soy‐lecithin, milk‐derived casein and bile salts (Siyal et al., 2017).

The complexities involved in the digestive process of dietary lipids; the age‐related physiological limitation of fat utilisation by young birds and the use of several dietary strategies to mitigate these shortcomings have been appreciated in previous literature that forms the background for this review (Ravindran & Abdollahi, 2021; Ravindran et al., 2016; Siyal et al., 2017). This review aims to link together these findings and revisit in detail the physiological responses resulting from the supplementation of exogenous emulsifiers in broiler diets as a plausible strategy for improved lipid utilisation.

2 | LIPIDS IN POULTRY NUTRITION

Lipids (fats and oils) constitute a wide variety of hydrocarbon substances that are insoluble in water but soluble in nonpolar organic solvents such as chloroform, ether, acetone and alcohol. Albeit erroneously, the term ‘fat’ has been generally used as a synonym for lipid. An effort has been made to ensure the accurate application of the two terms throughout the article. Although there is no internationally accepted classification for lipids, they can be broadly divided into three categories: simple, compound and derived (see Figure 2).

Simple lipids are esters of fatty acids with either glycerol, sterols or long‐chain monohydric alcohols (Gordon, 2003). They are the most abundant and are further subdivided into triglycerides, steroids and waxes (Baião & Lara, 2005). With a basic structure of three fatty acids and a monoacylglycerol, triglycerides constitute most of the lipids consumed by nonruminants (Rustan & Drevon, 2005). Upon hydrolysis, triglycerides are broken down into absorbable units of fat —two fatty acids and a monoglyceride.

Physiology of lipid digestion and absorption in poultry: An updated review on the supplementation of exogenous emulsifiers in broiler diets - Image 1

FIGURE 1 Important roles of lipids in diets and whole‐body metabolism. Source: Adapted from Oketch (2022).

FIGURE 2 General classification of lipids. Source: Adapted from Oketch (2022).

Compound (conjugated) lipids are esters of fatty acids and alcohol with nonlipid components such as minerals, protein and carbohydrates. They include phospholipids (together with phosphoric acid), glycolipids (bound to carbs) and lipoproteins from the association of lipids with proteins. With a hydrophobic core of phospholipids, cholesterol and apolipoproteins, lipoproteins are influential in vascular lipid transport. Table 1 contains the different classes of lipoproteins and their major components. Information about their associated apolipoproteins and the function of the major apoprotein (if known) is contained therein.

Derived lipids are obtained from the hydrolysis of simple and compound lipids. They include fatty acids, glycerol, sterols, alcohols, fat‐soluble vitamins (A, D, E, K), ketone bodies (acetone, acetoacetate and d‐3‐hydroxybutyrate) and terpenes. Depending on their chemical structure, fatty acids are classified as either saturated (single bonds) or unsaturated (two or more bonds). The names, number of double bonds and formulas of common fatty acids are presented in Table 2. Both α ‐linolenic acid (18:3 n ‐3) and linoleic acid (18:2 n ‐6) fatty acids are essential because their de‐novo synthesis is limited in chicken. Therefore, dietary provision of these fatty acids is essential due to their importance in growth and immune function (Balnave, 1970; Cherian, 2015; Swiatkiewicz et al., 2015).

To reduce costs while maintaining the caloric value of the feed, different fats and oils are added to poultry diets including yellow grease (recovered frying oil), rendering by‐products (lard, tallow, mutton and poultry fat), vegetable oils (safflower, perilla, soybean, maize, palm, among others) and acidulated soapstocks (Ravindran et al., 2016). For the fatty acid composition of commonly used fats and oils in animal feeding, the readers are directed to the tables presented by Pond et al. (2004) and Smink, (2012), showing that vegetable oils are richer in the more digestible unsaturated fatty acids whereas animal fats are abundant in saturated fatty acids.

In the context of constrained supply and price volatility, the interest in the utilisation of alternative nonconventional dietary lipid sources in broiler diets including insect‐based oils has increased (Kim et al., 2020; Patterson et al., 2021; Schiavone et al., 2018). The decision on the lipid (fat or oil) to use in the diet heavily depends on the availability and cost. Dietary lipid sources elicit a variety of responses in the broiler chicken, as has been reported (Baião & Lara, 2005) but with current technology, lipids are usually added at a level of not more than 4% in poultry diets because higher levels have a negative impact on pellet quality (Abdollahi et al., 2013).

TABLE 1 Different lipoprotein classes and their associated apoproteins

TABLE 2 Names, number of double bonds and formulas of common fatty acids.

Abbreviations: ALA, α‐linolenic acid; ARA, arachidonic acid; DHA, docosahexanoeic acid; DPA, docosapentanoeic acid; DTA, docosatetraenoic acid; EPA, eicosapentaenoic acid; LA, linoleic acid.

an‐7 and n‐9 monounsaturated fatty acids.

b n‐3 and n‐6 polyunsaturated fatty acids

Source: Adapted from Pond et al. (2004) and Smink (2012).

3 | DIGESTION OF LIPIDS IN POULTRY

It is well‐stated that the majority of lipids consumed by poultry are triglycerides and are insoluble in water. Thus, the function of the digestive process is to hydrolyse triglycerides into an absorbable form that is suitable for the aqueous environment of the small intestine. Feed goes through several processes in the gut including moistening, grinding, acidification, hydrolyzation, emulsification and the transport of end products (Klasing, 1999). This wide variety of processes enables the gut to carry out its main function—the digestion and absorption of nutrients (Celi et al., 2019). Upon reception by the beak, a subsequent decision by the tactile cells to reject or accept the feed is made depending on its reflectivity and taste with birds lacking the ability to smell. The ingested feed will be moistened and lubricated with saliva and watery mucus, respectively, and then propelled to either the proventriculus (glandular stomach) or the crop if the proventriculus is full. Up to this point, negligible action occurs toward fat digestion in poultry; unlike mammals, where lingual lipases initiate triacylglycerol digestion in the buccal cavity (Choi & Snider, 2019).

The digestion of dietary lipids is, therefore, initiated in the larger and multiwalled gizzard that is responsible for the mechanical breakdown (below 0.1 mm) and the vigorous mixing of feed. The proteolytic activity of pepsin in the gizzard and proventriculus helps to initiate the emulsification process by releasing lipids from cell wall matrices (Drackley, 2000). Additionally, the acidic environment and the churning activity of the gizzard further enhance the dispersion of lipids into a coarse emulsion. Another digestive mechanism that characterises lipid digestion in the gizzard is gut reflexes, which allows for the movement of the digesta (1) from the gizzard to the proventriculus; and (2) from the duodenum and jejunum back to the gizzard (Lentle et al., 2013; Sacranie et al., 2012). Through the continuous reverse peristaltic movement, the limitation of a shorter digestive tract is corrected thus, feed retention time is increased, allowing more time for digestion (Valaja & Siljander‐Rasi, 2001). The second flux of digesta movement from the duodenum and the jejunum introduces bile salts and monoglycerides to the gizzard effectively kickstarting the emulsification process. Additionally, the reflux of bile pigments from the small intestine gives the cuticular lining of the gizzard its characteristic green, brown or yellow colour (Klasing, 1999).

Passing the gizzard, partially emulsified lipid droplets together with chyme enter the upper small intestine (duodenum) through the pyloric sphincter. The arrival of lipid droplets in the small intestine stimulates the release of the hormone, cholecystokinin (CCK, Rao & Wang, 2010). CCK in turn stimulates the release of pancreatic and bile secretions that are crucial in fat digestion. Bile acid is formed in the liver, stored in the gallbladder and then delivered to the small intestine via two ducts (Dibner & Richards, 2004). It is largely made up of pigments, water, sodium salts, phospholipids, cholesterol, electrolytes and amino acids such as glycine and taurine. In poultry, taurine is the most predominant amino acid at 62% (Freeman, 1984; Tancharoenrat et al., 2022). The most important components for fat digestion in bile are sodium‐based salts and phospholipids. The conjugation of bile salts with taurine increases their solubility while reducing their toxicity, this makes them more efficient in forming mixed micelles (Ahn et al., 2003; Macdonald et al., 1983; Smallwood et al., 1972).

The amphipathic nature of bile salts reduces the tension at the oil‐water interface ensuring that the lipid particles that were initially reduced in size through the mechanical action of the gizzard are stable in the aqueous intestinal environment. This increases the surface area for pancreatic triacylglycerol lipase (PTL) to cleave lipids at the sn1‐ and sn3‐ positions leading to the release of two free fatty acids and sn‐2‐ monoacylglycerol (Tancharoenrat et al., 2014). About 97% of the bile salts will passively diffuse through the small intestine and then be recycled enterohepatically in the liver (De Boever & Verstraete, 1999; Macdonald et al., 1983). In addition, the alkaline nature of bile salts (pH 6) and the presence of sodium hydrogen carbonate in pancreatic juice creates an optimal alkaline environment for the action of PTL (around pH 7). Pancreatic juice is also known to contain co‐lipase, a protein co‐enzyme that complexes with lipase to form a more hydrophobic complex with an improved capacity to cleave lipids (Bauer et al., 2005). Co‐lipase is additionally involved in restoring the functioning of PTL, which could be inhibited by higher concentration of bile salts (Bosc‐Bierne et al., 1984).

Following the action of bile salts and pancreatic lipases, it has been reported that most of the dietary lipid digestion takes place in the jejunum around 75%, and to a lesser extent, in the duodenum around 15%–25% (Tancharoenrat et al., 2014). Fat digestion in the duodenum is limited to a preparative role due to the faster passage time (5–10 mins) in the broiler chicken (Ravindran, 2013a). Additionally, most fat absorption occurs in the jejunum, as will be later discussed in this review. Little or no digestion or absorption of lipids has been reported to take place in the lower ileum. Therefore, fat digestion and absorption in the hindgut (large intestine and ceca) have been termed negligible (Renner, 1965).

4 | ABSORPTION OF LIPIDS IN POULTRY

After fat digestion, free fatty acids and monoglycerides are directly absorbed by passive diffusion via the enterocytes without any need for emulsification and then transported while bound to serum albumin (Drackley, 2000). Due to limited lipogenesis in birds, the majority of fatty acids that will be transported to the adipose and muscle tissues are those that were directly absorbed through the plasma (Griffin et al., 1992). However, the absorption of medium and long‐chain fatty acids, diglycerides, fat‐soluble vitamins and cholesterol esters require the formation of mixed lipid‐bile salt micelles and continuous movement of lipids from the oil‐water interface of the intestinal lumen into the mixed micelles (Krogdahl, 1985).

Mixed micelles facilitate lipid absorption by accumulating lipolytic molecules at the unstirred aqueous layer close to the microvillus. The unstirred water layer has been implicated as a hindrance factor to efficient lipid absorption (Bauer et al., 2005; Brindley, 1984). There is considerable evidence alluding to the disruption of the micelles as facilitated by the low pH of the unstirred water layer before the uptake of both bile salts and lipids (Krogdahl, 1985; Shiau et al., 1985). The disruptive process allows for the separation of the bile salts from the micelles since the respective sites and mechanisms involved in the absorption of dietary lipids and bile salts are different (Drackley, 2000; Krogdahl, 1985). Bile salts are absorbed efficiently by active transport at the ileum and transported through the hepatic‐portal system to the liver (Lack & Weiner, 1961; Ahn et al., 2003); whereas dietary lipids are absorbed by passive diffusion at the jejunum (Tancharoenrat et al., 2014).

There is little doubt of passive fatty acid uptake into the cells after the disruption of the micelles however, the exact mechanism involved requires further elucidation. The absorption of fatty acids at the brush border membrane has been said to be a diffusional process that relies on the presence of a concentration gradient between the intestinal lumen and the epithelial cells (Drackley, 2000). The diffusional uptake of fatty acids could additionally be influenced by monoglycerides from the hydrolysis of the triglycerides (Ravindran et al., 2016). The intervention of low‐weight fatty acid‐binding proteins (FABPs) in fatty acid movement through the cytosol has also been reported (Ockner et al., 1972). Interestingly, the level of FABPs along the small intestine is influenced by the level of fat in the diet (Katongole & March, 1979). They noted that a low‐fat diet leads to higher FABP content at the duodenum with subsequent reductions posteriorly, whereas a higher‐fat diet, results in higher levels at the ileum. FABPs have a higher affinity for unsaturated fatty acids than saturated fatty acids, thus higher digestibility with dietary oils (Ockner & Manning, 1974). Besides the degree of saturation, fatty acid absorption rates are generally dependent on the chain length; decreased digestibility is a function of increased chain lengths (Xu et al., 2021).

Most of the absorbed fatty acids will then go through the monoglyceride pathway before being transported to other organs. The pathway allows for the reesterification and assembly of cholesterol and phospholipids together with the nonpolar lipids into larger lipoprotein molecules including chylomicrons (see Table 1). It is in a mammalian chylomicron‐like form called portomicron (85%–95% triglycerides) that lipids are transported in the chicken blood through the portal vein to the liver (Griffin et al., 1992). To facilitate the uptake and metabolism of its contents, the portomicron surface is lined with protruding apolipoproteins such as apoE, apoB‐48, apoC‐II, apoC‐III and apoA‐IV (see Table 1). It is plausible that portomicrons could be too large to be metabolised by the liver thus they are readily cleaved by lipoprotein lipase (upon activation by apolipoprotein C‐II) at the sn‐1 and sn‐3 positions; two free fatty acids and sn‐2‐ monoacylglycerols are produced as end products. The free fatty acids will be transported to the muscle tissues via the capillaries and in the case of the adipose tissue, they are reesterified and stored as triglycerides, whereas the portomicron remnants, which are largely cholesterol and proteins (Apo A‐I and apolipoprotein B‐100), will go through apoE‐mediated endocytosis in the liver (Cooper, 1997).

Lipid digestion and absorption are influenced by several bird and diet‐related factors (Ravindran et al., 2016). The digestive utilisation of lipids is significantly more complex than those of other macronutrients; and is dependent on the supply of adequate amounts of bile salts, PTL and co‐lipase. Generally, the digestion and absorption of lipids which are mostly triglycerides in poultry involve the breakdown of large droplets, emulsification, lipolysis by pancreatic lipase and micelle formation. Subsequently follows, micelle disruption, the absorption and the reassembly of FA into large lipoprotein particles that will then be acted upon by lipoprotein lipase; to produce FA and monoglycerides that can be stored in tissues or used as a source of energy.

5 | DIGESTIVE LIMITATION OF LIPIDS IN YOUNG CHICKS

Due to intensive genetic selection for muscle production, the growth potential and the feed conversion efficiency of the modern broiler have been optimised greatly (Zuidhof et al., 2014). This necessitates the provision of easily digestible and nutrient‐dense diets that maximises the genetic potential of modern, high‐performing broilers. Therefore, during the first few days, the posthatch chick has to deal with a transition from a yolk‐based lipid nutrient supply to an exogenous diet that is predominantly carbohydrate‐based; a shift to aerial breathing; and the beginning of independent thermal regulation (Christensen, 2009; Wong & Uni, 2021). It is well known that growth during the first week has a huge effect on the survival and performance of the flock (Noy & Uni, 2010; Yassin et al., 2009). With ideal management, modern broilers can achieve a maximal relative growth rate in the excess of 300% from an initial weight of around 44 g to more than 200 g during the first week (Aviagen, 2022).

The attainment of such a rapid growth rate calls for an equally quick adaptive response in dealing with stressors and negating the physiological immaturity of the gastrointestinal tract while still being able to acquire, digest and utilise nutrients (Ravindran & Abdollahi, 2021). Therefore, in an adaptive response to the increase in solid feed consumption, the intestinal mass for the proventriculus, gizzard and small intestine (duodenum, jejunum and ileum) increases rapidly relative to the body weight, especially in the first week after hatch (Nir et al., 1993; Noy & Sklan, 1997). Additionally, the intestinal mucosa undergoes profound changes with increases in villus size, volume and complexity as has been reported (Uni et al., 1995). Due to the consumption of solid feed and the rapid increase in the size and complexity of intestinal organs, there is a subsequent increase in the total digestive enzyme activity of lipase, amylase, trypsin and chymotrypsin (Noy & Sklan, 1995).

Nonetheless, the reported increases in the total digestive enzyme activity, particularly for lipase (the enzyme responsible for lipolysis), may be too inadequate to match the total feed intake (Jin et al., 1998; Nitsan et al., 1991; Noy & Sklan, 1997). In addition, the maximal increase in the secretion of pancreatic lipase takes longer to plateau, around 10–16 days, when compared to other digestive enzymes such as amylase, trypsin and chymotrypsin whose production maximises earlier at 4–7 days post-hatch (Nir et al., 1993; Noy & Sklan, 1997). The age‐related depression in the secretion of endogenous pancreatic lipase production is also occasioned by limited production of FABPs, and bile salts which are directly involved in lipid utilisation as previously discussed. Therefore, an age‐related physiological limitation in the capacity of young birds to utilise lipids effectively, particularly saturated animal fats has been reported (Leeson & Atteh, 1995; Oketch et al., 2022). Tancharoenrat et al. (2013) demonstrated an age‐related depression in the capacity of newly hatched birds to digest and utilise lipids effectively, more so during the first week.

The limited fat utilisation capability of young chicks is exacerbated by the delayed access to feed post-hatch which is commonplace in the practical setting and the stress from post-hatch handling and transport (Prabakar et al., 2016; Uni et al., 1998; Wang et al., 2014). Therefore, it has been of particular importance for nutritionists to explore strategies aimed at optimising the energy‐yielding potential of dietary lipids. Several strategies have been investigated including the blending of saturated and unsaturated fats to maximise the natural emulsifying effects of unsaturated fats; feed processing through steam cooking; lowering the Ca content to prevent lipophytin (Ca/Mg‐phytate, lipids and peptide complex) formation; use of supplemental enzymes (lipases and glucanases); and last, the use of exogenous emulsifiers whose attention is drawn to in the current review for their relevance in broiler diets (Meng et al., 2004; Ravindran et al., 2016).

6 | APPLICATION OF EXOGENOUS EMULSIFIERS

Exogenous emulsifiers are molecular surfactants with both hydrophobic and hydrophilic properties (Bai et al., 2019). The hydrophobic end with fatty acids is directed to the oil phase, while the hydrophilic end with sucrose, glycol, glycerol, sorbitol or polyglycerol is directed to the aqueous phase forming a ‘molecular bridge’ that inhibits the coalescing of hydrolysed lipid droplets into large molecules. Being surface‐active substances, they reduce the surface tension at the oil‐water interface allowing for the efficient formation and stabilisation of emulsions; and the efficient suspension of lipolytic molecules in the formed emulsions (Upadhaya et al., 2019).

Emulsifiers are widely used in the food industry as an additive to stabilise lipids in the food matrix. The main food products that utilise emulsifiers are mayonnaise, margarine, creamy sauces, ice cream and baked goods. Additionally, emulsifier products are widely used in the production of agrochemicals, personal care products, supplements, pharmaceuticals and cosmetics (McClements & Jafari, 2018). Emulsifiers have also been widely utilised in the animal production industry as one of the strategies aimed at improving lipid utilisation. Emulsifier products could be natural or synthetic in nature. Natural emulsifiers could include bile, phospholipids, soy lecithin and casein, while synthetic emulsifiers could include lysolecithin, glycerol monostearate, glycerol distearate, sodium stearoyl‐2‐lactylate, among others (Siyal et al., 2017).

Emulsifier effects are largely dependent on the hydrophilic‐lipophilic balance (HLB) which determines the extent of fat or water solubility. The HLB value ranges from 0 to 20, with low HLB representing improved fat solubility in oil‐in‐water emulsions and high HLB signifying improved water solubility in water‐in‐oil emulsions. Based on Bancroft's rule that an emulsifier should be soluble in the continuous (aqueous phase), a high HLB emulsifier is desirable. This is because the small intestinal environment is predominantly aqueous and birds are known to consume almost twice as much water as feed (Bancroft, 1912; Ravindran, 2013b; Siyal et al., 2017). The efficacy of dietary emulsifiers varies depending on the levels and source of fat; and the metabolisable energy levels (Tenório et al., 2022).

Taken together, the use of exogenous emulsifiers, as will be later discussed in this review, improves fat digestibility and the overall energy efficiency of diets. They could also confer gut health‐promoting, neuroprotective and antioxidative properties (Brautigan et al., 2017; Ho Cho et al., 2012; Saleh et al., 2020). In practical terms, dietary emulsifier supplementation could allow for the incorporation of fats and oils into lower‐energy diets without compromising on broiler performance with the potentiality of relatively lowered feed costs thus, more economic gains (Siyal et al., 2017). A broader discussion on the physiological responses of broiler chickens to exogenous emulsifier supplementation in fat and oil‐incorporated diets is hereby presented.

6.1 | Growth performance

A summary of the commonly used emulsifiers and their varying physiological effects, when used in fat‐infused broiler diets, is contained in Table 3. Under the limitation of a constrained supply of conventional feed resources such as corn (Aho, 2007), the addition of dietary lipids provides a plausible alternative to meeting the energy requirements of high‐performing modern broilers. However, due to the previously mentioned physiological limitations, lipid digestion by the young chick is limited. Emulsifier supplementation during the early stages of chicks' development could confer incremental effects on body weight gain and feed efficiency when fat‐incorporated reduced energy diets are fed and, thus has been exhaustively reported (Ho Cho et al., 2012; Upadhaya et al., 2017; Wang et al., 2016). An additional investigation conducted by Bontempo et al. (2018) reported that the use of glycerol PEGR in broiler diets resulted in improved body weights, daily weight gains and feed efficiency. The widely observed improvements in the indices of growth performance are attributed to several factors including improved nutrient digestibility and higher energy efficiency of the diets with emulsifiers supplementation. This could impart a mitigating effect on the depressed growth performance that has been recorded for birds fed fat‐incorporated reduced energy diets without emulsifiers (Oketch et al., 2022).

Notably, discrepancies in broiler growth performance with dietary emulsifiers have also been reported (Guerreiro Neto et al., 2011; Shen et al., 2021; Zampiga et al., 2016). The differences could result from the varying efficacy of emulsifiers in line with their HLB, supplemental lipase use, and probably, the type and level of lipids in the basal diets (Jansen et al., 2015; Siyal et al., 2017; Solbi et al., 2021). Nevertheless, the possibility of lowered feed costs and potentially more economic gains, through the use of dietary exogenous emulsifiers without compromising on broiler performance has been explored (Siyal et al. (2017). A recent meta‐analysis by Wealleans et al. (2020) analysed the effect of lysolecithin‐based products across different fat levels and sources with the addition of dietary lipids at approximately 4.42%. They determined that the supplementation of lysolecithin‐based products at 125 and 250 g/ tonne could replace 57.88 and 73.11 kcal/kg of feed respectively. The supplementation of the lysolecithin emulsifier at 125 g/tonne and above to improve feed efficiency was concluded.

6.2 | Nutrient digestibility

Due to their amphipathic properties, the capacity of different exogenous emulsifiers to improve the ether extract digestibility of fat‐incorporated reduced energy diets has been widely reported (Dabbou et al., 2019; Polin et al., 1980; Roy et al., 2010). Using sodium stearoyl‐1, 2‐lactylate together with tween at 0.05%, Serpunja and Kim (2019) reported improved digestibility of fat. Considering the significant improvements in fat digestibility, emulsifiers have been associated with increasing the active surface area for lipase to hydrolyse triglyceride molecules into fatty acids and monoglycerides, and the subsequent formation of mixed‐lipid bile salt micelles. Due to an optimised lipolysis and micelle formation process, dietary emulsifiers could impart a corrective effect on fat maldigestion and malabsorption that has been exhaustively reported in young birds (Tancharoenrat, 2012). Dietary exogenous emulsifiers have also been reported to exert ‘beyond‐lipid effects’ with improvements in the digestibility of crude protein (Boontiam et al., 2017; Haetinger et al., 2021), energy (An et al., 2020; Park et al., 2018) and dry matter (Oketch et al., 2022; Upadhaya et al., 2018; Zhao & Kim, 2017). The overall improvements in nutrient digestibility are attributed to a probable alteration of the phospholipid bilayer of cell membranes for enhanced nutrient uptake (Lundbæk et al., 2009).

TABLE 3 Physiological responses of broilers to exogenous emulsifier supplementation in fat‐incorporated diets.

Note: ↑ means increase and ↓ means decrease.

Abbreviations: ADFI, average daily feed intake; ADG, average daily gain; AMEn, nitrogen‐corrected apparent metabolisable energy; ASO, acid soybean oil; ATTD, apparent total tract digestibility; BW, body weight; CA7, carbonic anhydrase VII; CD36, cluster of differentiation 36; CP, crude protein; CSL, calcium stearoyl‐2 lactylate; DM, dry matter; DSO, degummed soybean oil; EE, ether extract; FCR, feed conversion ratio; FSO, flaxseed oil; HAVFs, hydrogenated animal and vegetable fats; HDL‐C, high‐density lipoprotein cholesterol; IL‐1β, interleukin‐1 beta; IL‐8, interleukin 8; LDL‐C, low‐density lipoprotein cholesterol; NDV, Newcastle disease virus; PEGR, glycerol polyethylene glycol ricinoleate; PF, poultry fat; PFP, palm fat powder; SFF, soybean full fat; SFFA, soy‐free fatty acids; SO, soybean oil; SRBC, sheep red blood cells; SSL, sesame seed oils; SSO sesame seed oil; TBARS, thiobarbituric acid reactive substances; TTNR, total tract nutrient retention; WHC, water‐holding capacity.

6.3 | Blood metabolites

Previous investigations on emulsifier effects on some blood metabolites have largely reported lowered plasma cholesterol and triglyceride concentration (Huang et al., 2007; Roy et al., 2010; Zhao & Kim, 2017). The reduction effect of dietary emulsifiers on serum cholesterol and triglyceride concentrations has been attributed to a rapid elimination rate of chylomicrons from blood (Roy et al., 2010). This could be due to possible emulsifier improvements in the hydrolysing action of lipoprotein lipase (upon activation by apolipoprotein C‐II) at the sn‐1 and sn‐3 positions; to release two free fatty acids and sn‐2‐ monoacylglycerols from triglycerides that are sequestered in chylomicrons. The hypothesis of rapid chylomicron removal has been corroborated by reports of higher lipoprotein lipase with dietary emulsifiers (Ge et al., 2019; Lai et al., 2018).

Another possible mechanism for the reduced cholesterol and triglyceride levels with dietary emulsifiers is through the suggested stabilisation of the phospholipid coating of chylomicrons (Jones et al., 1992). This could, in turn, decrease the secretion rate of cholesterol and triacylglycerols into the blood (Oketch et al., 2022). Further studies should elucidate the mechanisms behind the lowering effect of emulsifiers on some blood metabolites; even though some inconsistencies with elevated total cholesterol levels have also been reported in previous publications (Bontempo et al., 2018; Saleh et al., 2020).

Increased levels of other blood plasma metabolites including globulins and lipase have been reported (Oketch et al., 2022; Saleh et al., 2020 respectively). It has been hypothesised that higher levels of lower fat particles within the gut could lead to increased lipase demand (Guerreiro Neto et al., 2011). The increased lipase activity could be directly associated with the ripple effect of improved lipid digestibility that has been recorded with emulsifiers (Oketch et al., 2022). Furthermore, higher globulin levels in the serum that could be representative of improved immune function with dietary emulsifiers have been reported elsewhere (Ho Cho et al., 2012; Saleh et al., 2020).

6.4 | Ileal histomorphology and gut health

Concerning the morphology and general physiology of the gut, emulsifiers have been reported to trigger epithelial changes that improve nutrient digestibility and overall gut health (Boontiam et al., 2017; Brautigan et al., 2017). Gut health will be considered as the general existence of a stable and coordinated interaction between the diet, commensal microbiome, intestinal mucosa and immune system in a symbiotic equilibrium that allows the gut to carry out its physiological functions, maintain homoeostasis and withstand stressors. Wickramasuriya, Macelline, et al. (2020) reported that the dietary feeding of emulsifiers alongside lipases resulted in longer villus heights (VH), deeper crypt depth (CD), and higher VH:CD ratios (see Table 3). Such improvements could translate to enhanced intestinal absorption activity. Marginal improvements in the villus absorptive surface area have also been reported (Oketch et al., 2022). The morphological improvements could result from the synergistic interactions of feed ingredients including dietary emulsifiers as opposed to the influence of the emulsifier in isolation (Brautigan et al., 2017).

Furthermore, Cloft et al. (2021) reported that the addition of lysolecithin led to the upregulation of carbonic anhydrase VII and interleukin 8‐like 2, which have been also associated with better gut health (see Table 3). However, variations could also exist with no significant effects of emulsifiers on gut morphology being previously reported (Tenório et al., 2022; Wickramasuriya, Cho, et al., 2020). Concerning the vital role of the microbiota as an integral part of the gut health nexus alongside the diet, mucosa and immune system, further investigations on emulsifier effects on intestinal microbiota could be necessary. Kubiś et al. (2020) reported the ability of glycerol PEGR to reduce caecal Clostridium populations in a synergistic response with xylanase in tallow‐incorporated diets. Additionally, Shen et al. (2021) reported that soy‐lecithin use at 0 and 1 g/kg could lead to lower Firmicutes and higher Bacteroidetes levels. The impact of lower Firmicutes could be associated with leanness which explains the reduced levels of abdominal fat deposition that was reported with emulsifiers in the current study by Shen et al. (2021) and elsewhere too (Haetinger et al., 2021; Lai et al., 2018).

6.5 | Viscera organ weights

Dietary emulsifier supplementation has been reported to improve liver and pancreas weights alluding to increased function, in terms of lipid biosynthesis and metabolism (Boontiam et al., 2017; Oketch et al., 2022; Wickramasuriya, Macelline, et al., 2020). The liver is vital in the cholesterol conversion to bile salts; and the apoE‐mediated endocytic clearance of chylomicron remnants including cholesterol and apoproteins (Apo A‐I and B). Being the principal site of lipid biosynthesis in birds, the liver is also involved in the secretion of the main classes of lipoprotein particles including high‐density lipoprotein (HDL) and very low‐density lipoprotein; and their major associated apoproteins namely Apo A‐I and Apo B‐100 respectively (Hermier, 1997). The assertions of improved lipid biosynthesis activity have been corroborated by the reports of increased HDL‐cholesterol with dietary emulsifiers (Bontempo et al., 2018; Saleh et al., 2020, see Table 3). Future investigations on the impact of emulsifiers on liver lipid biosynthesis could be supported by data on the lipoprotein components including HDL‐cholesterol. Additional studies on the expression of apoproteins associated with chylomicrons assembly and transport (apoE, apoB‐48, apoC‐II, apoC‐III and apoA‐IV) are imperative. To the best of the authors' knowledge, only Bontempo et al. (2018) have investigated gene expression in the liver with emulsifiers to date; however, no significant effects on the expression of Apo A‐I and Apo B‐100 were reported.

The overall intervention of biosurfactants in the immunological process has been effectively alluded to with reports of reduced levels of proinflammatory cytokines (Hartmann et al., 2009; Yun et al., 2005; Zhao et al., 2011). Emulsifier supplementation in broiler diets had a beneficial effect on the bursa of Fabricius weights as has been reported (Ho Cho et al., 2012). Such increments could translate to improved humoral immune function (Yvernogeau et al., 2022); even though further investigations are important to verify such an effect. Furthermore, Allahyari‐Bake and Jahanian (2017) reported that broilers supplemented with lysolecithin recorded higher bursa of Fabricius weights; and improved antibody production titre against infectious bursal disease, sheep red blood cells, Gumboro and Newcastle disease virus. Notably, spleen weight reductions that could allude to an immunosuppressive effect with emulsifiers have also been reported (Ho Cho et al., 2012; Upadhaya et al., 2018). Due to the reported inconsistencies, the overall impact of emulsifier effects on immunological organs (thymus, spleen and bursa of Fabricius) is still unclear, thus further investigations are imperative. Such data could be supported by studies on some of the plasma metabolites related to the immune system including globulins that have been reported to be increased with dietary emulsifiers (Saleh et al., 2020).

6.6 | Carcass traits and meat quality

Dietary emulsifiers improved breast and carcass percentages as has been previously reported (Boontiam et al., 2017; Ge et al., 2019). Furthermore, Lai et al. (2018) reported that the use of bile acids in lard‐incorporated diets could lead to higher dressing and thigh muscle percentages. Some of the reported improvements reflect positively on carcass quality in terms of lower abdominal fat percentages (Haetinger et al., 2021; Lai et al., 2018; Shen et al., 2021). This could impart a corrective effect on excessive fat deposition due to the common use of energy‐dense diets with reported wastages at the slaughterhouse level (Fan et al., 2008; Fouad & El‐Senousey, 2014; Zaman et al., 2008).

Using bile acids (hyodeoxycholic acid, 19.61% chenodeoxycholic acid and 8.00% hyocholic acid), Ge et al. (2019) showed that the use of a lower energy diet at 2940 kcal/kg and emulsifiers lowered the abdominal fat percentage of broilers at Day 42. The reduced abdominal fat percentages that were noticed with lower energy levels have been attributed to reduced activity levels of enzymes such as fatty acid synthase, which are involved in de‐novo lipogenesis (Tanaka et al., 1983). However, due to differences in the efficacies of emulsifiers, inconsistent results in terms of increased abdominal fat levels have also been reported (Wang et al., 2016).

Concerning meat quality, several studies have reported improved muscle yellowness with dietary emulsifiers (Oketch et al., 2022; Upadhaya et al., 2017; Wickramasuriya, Macelline, et al., 2020). The observation could be due to a probable involvement of emulsifiers in the accumulation of lipid‐soluble pigments responsible for yellowness, such as xanthophylls as has been alluded to by Laudadio and Tufarelli (2011). Further evidence of increased meat tenderness as indicated by a lowered shearing force with dietary emulsifiers has also been reported (An et al., 2020). Dietary emulsifier supplementation has also resulted in lowered thiobarbituric acid reactive substances levels that are concomitant to reduced lipid peroxidation and oxidative stress. This suggests that dietary emulsifiers could exert desirable antioxidative properties (Saleh et al., 2020). Due to elevated consumer interest and industry standards, the impact of feed additives including emulsifiers on the final meat quality is far from conclusive, and thus, future investigations are critical.

7 | CONCLUSIONS

Alongside other important roles, lipids provide a plausible alternative at relatively lowering feed costs while increasing the energy density of diets for modern fast‐growing broilers. However, lipid digestion and utilisation are much more complex than that of the other macronutrients. An age‐related physiological limitation in the capacity of newly hatched birds to utilise lipids effectively, particularly animal fats, has also been reported. Based on the evidence presented in the current review, exogenous emulsifier supplementation in fat‐infused diets as a strategy for improved lipid utilisation improves ether extract digestibility and broiler growth performance. In practical terms, emulsifiers allow for the incorporation of lipids into reduced energy diets without compromising on broiler performance with the potentiality of relatively lowered feed costs, thus, more economic gains. Notably, some unequivocal physiological responses from dietary emulsifier supplementation have also been reported. For robust understanding of emulsifiers, further studies are imperative on blood metabolites related to fat metabolism; liver gene expression; meat quality; immunological organs and gut microbiota of broilers. Notably, such measurements should be supported with data on fat digestibility; and productive indices such as growth performance, carcass yields and muscle quality. The investigation of potential synergies resulting from dietary emulsifiers alongside other strategies for improved fat utilisation such as lipases and glucanases are also necessary.

This article was originally published in Journal of Animal Physiology and Animal Nutrition, 2023;1–15. DOI: 10.1111/jpn.13859. This is an Open Access article under the terms of the Creative Commons Attribution‐NonCommercial License.