All emerging data on bioactive compounds in eggs and factors influencing nutritional value in eggs of various domestic species
The egg is an encapsulated source of macro and micronutrients that meet all the requirements to support embryonic development until hatching.
The perfect balance and diversity of its nutrients along with its high digestibility and affordable price have put the egg in the spotlight as a basic food for humans.
5 Myths About Eggs Debunked and Everything You Need to Know About Them Today
Most experimental, clinical and epidemiological studies concluded that there was no evidence of a correlation between dietary cholesterol from eggs and an increase in total plasma cholesterol. Egg remains a high nutritional quality food product for adults, including the elderly and children, and is widely consumed worldwide. In parallel, there is convincing evidence that egg also contains many bioactive compounds yet unexplored, which may be of great interest in disease prevention/treatment. This article will provide:
- An overview of the main nutritional characteristics of the hen's egg
- All emerging data on bioactive compounds in eggs
- Some factors that influence the composition of eggs, including a comparison of the nutritional value of eggs from various domestic species
1. Introduction
In 1968, the egg industry faced recommendations from the American Heart Association that encouraged people to consume fewer than three whole eggs per week, claiming that high dietary cholesterol was related to high blood cholesterol and therefore higher risks of cardiovascular disease. These recommendations not only impacted the egg industry, but also affected people's eating habits in part by depriving them of a convenient and nutritionally valuable food. In 1995, there was a concerted effort to unify all U.S. national dietary recommendations and to support in vitro and in vivo research to rehabilitate eggs. [ 1 ]. Half a century of research has now shown that egg intake is not associated with increased health risks. [ 2 ] and that it is worth incorporating this product into our diet for its high nutrient content and its numerous bioactivities [ 1 ]. Some recent research has highlighted the beneficial role of eggs for humans, including physically active people, and several authors have demonstrated that Egg cholesterol is not absorbed well [ 3 , 4 ]. Consequently, egg consumption does not have a significant impact on blood cholesterol concentrations. [ 3 , 4 ]. In parallel, egg consumers, especially children aged 6–24 months, eat lower total and added sugars than non-consumers [ 5 ], which is probably related to its satiety effect [ 2 , 6 , 7 ]. It is now well established that the egg can contribute to general health throughout life, although people suffering from metabolic disorders such as diabetes, hypercholesterolemia and hypertension still need to pay attention to their dietary cholesterol intake [ 8 ].
Another concern is egg allergy, which is a common food allergy with an estimated prevalence of 1.8% to 2% in children younger than five years. Molecules associated with egg hypersensitivity are mainly concentrated in the egg white, with ovalbumin, lysozyme, ovomucoid, and ovotransferrin being the major egg allergens [ 9 ]. Some yolk-derived proteins have also been reported [ 9 ]. Egg allergy usually develops within the first five years of life, with 50% of children outgrowing egg hypersensitivity by age three [ 10 , 11 ]. Fortunately, in most cases, the prevalence of egg allergy decreases with age [ 12 ] and usually resolves by school age.
Eggs are of particular interest from a nutritional point of view, they contain essential lipids, proteins, vitamins, minerals and trace elements [ 13 ], offer a moderate caloric source (about 140 kcal/100 g), a great culinary potential and a low economic cost. In fact, Eggs have been identified as the cheapest animal source of protein, vitamin A, iron, vitamin B12, riboflavin, choline and the second cheapest source of zinc and calcium [ 14 ]. In addition to providing well-balanced nutrients for infants and adults, the egg contains a myriad of biologically active components [ 15 , 16 , 17 ]. These components are allocated in the various internal components of the egg ( Figure 1 ). It should be mentioned that the eggshell and its closely associated eggshell membranes are usually not consumed, although the eggshell membranes are edible ( Figure 1 ). The average consumption of eggs/year/capita in the world ranges from 62 (India) to more than 358 (Mexico) [ 18 ] and it is even lower in African countries (36 eggs/year/capita) ([ 19 ]. and are produced by approximately 3 billion hens , raised around the world specifically for human consumption.
Egg components are also reported to be highly digestible although a small amount of egg proteins is not assimilated [ 20 ], especially when egg is consumed as a raw ingredient [ 20 , 21 , 22 ]. The higher digestibility of cooked egg proteins results from heating-induced structural protein denaturation, thus facilitating the hydrolytic action of digestive enzymes. However, although egg protein assimilation is facilitated by heat pretreatment and to a high level (91–94% for cooked egg white proteins), it remains partially incomplete. Interestingly, major proteins, essentially egg white proteins such as ovomucoid proteinase inhibitor and egg white major ovalbumin resist thermal heating [ 23 , 24 ]. This observation is particularly interesting, knowing that egg-derived proteins and many hydrolytic peptides generated in vitro by limited digestion of egg white proteins possess biological activities of interest for human health and can therefore be used as nutraceuticals [ 16 ]. Indeed, many of these have been shown to exhibit antimicrobial, antioxidant and antitumor properties [ 25 , 26 , 27 ]. Therefore, many authors have highlighted the importance of protein-derived peptides in the intestine and their substantial role in the first line of immunological defense of the organism, in immune regulation and in the normal functioning of the body [ 28 ].
2. Nutrients for eggs
Egg proteins are equally distributed between egg white and egg yolk, while lipids, vitamins and minerals are essentially concentrated in egg yolk ( figure 2 ). Water constitutes the majority of eggs ( figure 2 ) and it is interesting to note that the egg is devoid of fibre. The relative content of egg minerals, vitamins or specific fatty acids may vary from one national reference to another [ 29 ] but remains globally comparable when considering the main constituents such as water, proteins, lipids and carbohydrates. The main nutrients of eggs are, in fact, very stable and depend on the ratio between egg white and yolk in contrast to the minor components, which are influenced by several factors, including the hens' diet (see section 4.2 ). Taken together, raw and freshly laid eggs, water, protein, fat, carbohydrates and ash account for approximately 76.1%, 12.6%, 9.5%, 0.7% and 1.1% respectively [ 30 ].
Basic composition of edible parts of the egg. ( a ) Egg white; ( b ) Egg yolk. Note that for ( b ), the results refer to the egg yolk/yolk membrane complex. Retrieved 11/01/2019 from the Ciqual homepage https://ciqual.anses.fr/ (French Agency for Food, Environmental and Occupational Health and Safety. ANSES-CIQUAL).
2.1. Macronutrients
2.1.1. proteins
Egg white and egg yolk are highly concentrated in proteins. Hundreds of different proteins have been identified, associated with specific physiological functions to meet specific time requirements during embryonic development. The compartment specificity of some of these proteins can be explained by the fact that egg yolk and egg white are formed from distinct tissues. Egg yolk is essentially of hepatic origin, while egg white is synthesized and secreted after ovulation of the mature yolk in the oviduct of the hen [ 31 ].
The protein concentration is, on average, 12.5 g per 100 g of raw whole fresh egg, while the egg yolk with its vitelline membrane and the albumen contain 15.9 g protein and 10.90 g protein per 100 g, respectively. These values are slightly modified by the hen's genetics and age (see Section 4 ). Thanks to complementary proteomic approaches, almost 1000 different proteins have been identified in the hen's egg, including the eggshell [ 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 ].
The yolk is a complex medium containing 68% low-density lipoproteins (LDL), 16% high-density lipoproteins (HDL), 10% livetins and other soluble proteins, and 4% phosvitins. These components are distributed between insoluble protein aggregates called granules (19–23% of the dry matter), which represent about 50% of the yolk proteins, and a light yellow fluid or plasma, which corresponds to 77–81% of the dry matter [ 41 , 42 ]. Apolipoprotein B, apovitellenin-1, vitellogenins, serum albumin, immunoglobulins, ovalbumin, and ovotransferrin are the most abundant proteins in egg yolk, accounting for more than 80% of the total egg yolk proteins. [ 43 ]. The yolk is closely associated with the vitelline membranes, which consist of two distinct layers [ 44 ] that form an extracellular protein matrix that surrounds the yolk. These membranes provide the yolk with a physical separation from the other compartments of the egg and prevent subsequent leakage of the yolk into the albumen.
Egg white is a lipid-free gelatinous structure and is composed mainly of water (about 88%) [ 44 ] ( figure 2 ), fibrous structural proteins (ovomucins), glycoproteins (ovalbumin, protease inhibitors), antibacterial proteins (lysozyme) and peptides (see Section 3.1 ) [ 33 , 45 ].
The average volume of albumen is estimated at 30 ml (for an egg weighing 60 g, eggshell included) and the protein concentration is approximately 110 mg/ml of albumen. In total, 150 distinct proteins have been identified in egg albumen . [ 35 ], knowing that the abundant ovalbumin represents 50% of the total albumen protein. The physiological function of this protein in the egg remains unknown, but Ovalbumin is assumed to provide essential amino acids for the growth of the chicken embryo . Egg white is therefore a valuable source of amino acids for human nutrition. In addition to ovalbumin, Egg white is concentrated in the antibacterial lysozyme which is currently used as an anti-infective agent in many pharmaceutical products and as a food preservative ( see Section 3.1 ). The viscous appearance of egg white is essentially due to ovomucin [ 46 ]. Surprisingly, egg white is also characterized by the presence of four highly abundant protease inhibitors [ 47 ] which can delay the digestion of egg components, especially when egg white is used as a raw ingredient in some food preparations.
2.1.2. Lipids
The total lipid content is relatively stable in the egg and ranges from 8.7 to 11.2 per 100 g of whole egg, considering various EU countries and US egg composition tables [ 29 ]. These lipids are concentrated only in the egg yolk ( Figure 2 and Table 1 ) and a small part may remain closely associated with the vitelline membranes [ 48 , 49 ].
Egg lipids
Lipids are part of the yolk lipoproteins whose structure consists of a core of triglycerides and cholesterol esters, surrounded by a monolayer of phospholipids and cholesterol in which apoproteins are incorporated [ 42 ]. It is very difficult to change the total lipid content in the egg. An increase in fat in the egg depends essentially on the increase in the yolk/albumen ratio, which however is scarcely influenced by the hen's diet. On the contrary, The fatty acid profile is highly dependent on the hen's diet (see paragraph 4.2 ). This variability is illustrated in the Table 1 from minimum and maximum values of fatty acids (saturated, monounsaturated and polyunsaturated). In particular, the relative amount of unsaturated (monounsaturated + polyunsaturated) and saturated fatty acids in the yolk (5.31 g versus 2.64 g per 100 g of whole egg, Table 1 ) is particularly high compared to other food sources of animal origin. The yolk is also a rich source of essential fatty acids such as linoleic acid (FA 18:2 9c,12c (n-6)). The high cholesterol content of eggs (400 mg per 100 g of whole egg) contributed to the decline in egg intake 30 to 40 years ago, although many studies conducted in the 1990s reported an absence of correlation between egg intake and high plasma cholesterol levels [ 3 , 4 ]. It is now assumed that the variation in plasma cholesterol and the associated cardiovascular disease risk results from dietary factors but also from the intake of saturated fatty acids (such as myristic (14:0) and palmitic (16:0) acids in the diet). Older in vivo studies in monkeys and gerbils have shown that 14:0 (myristic acid) and 18:2 (linoleic acid) are the major fatty acids modulating plasma cholesterol: 14:0 was the major saturated fatty acid increasing plasma cholesterol and 18:2 was the only fatty acid that consistently lowered it [ 50 , 51 ]. In egg, 14:0 (myristic acid, 0.024 g per 100 g whole egg) is much less concentrated than the unsaturated fatty acid 18:2 (linoleic acid, 1.38 g per 100 g whole egg). All these data agree in confirming that the egg is not associated with a higher incidence of cardiovascular disease in healthy patients. However, egg intake should be monitored in hyper-responders to dietary cholesterol (about 15% to 25% of the population), since an increase in egg consumption in these people affects plasma lipids to a greater extent than in hypo-responders.
2.1.3. Carbohydrates
The egg does not contain fiber and its carbohydrate content is low (0.7%). Egg carbohydrates are distributed between egg yolk and egg white ( figure 2 ). Glucose is the dominant free sugar in the egg (about 0.37 g per 100 g of whole egg) and is essentially present in the egg white (0.34 g per 100 g of egg white versus 0.18 g per 100 g of yolk) [ 30 ]. Traces of fructose, lactose, maltose and galactose have been detected in raw egg white and raw egg yolk [ 30 ]. Carbohydrates are also highly represented in egg proteins, knowing that many of them are glycoproteins that undergo post-translational glycosylations before secretion by the reproductive tissues of the hen to form yolk, membranes and egg white.
2.2. Micronutrients
2.2.1. Vitamins and choline
The egg, and more specifically the egg yolk, is a vitamin-rich food containing all vitamins except vitamin C (ascorbic acid). The absence of vitamin C in the egg may be due to the fact that birds are able to meet their vitamin C requirement by de novo synthesis from glucose [ 52 ]. The ability to produce vitamin C has been lost during the evolutionary process in several animal species including guinea pigs, monkeys, flying mammals, humans and some evolved passerine birds [ 52 ]. Consequently, the latter species, but not domestic birds, are dependent on dietary sources of vitamin C (fruits and vegetables). The egg yolk contains a high amount of vitamins A, D, E, K, B1, B2, B5, B6, B9 and B12, while the egg white has high amounts of vitamins B2, B3 and B5 but also significant amounts of vitamins B1, B6, B8, B9 and B12 ( Table 2 ). Eating two eggs a day covers 10% to 30% of the vitamin requirement for humans. It is interesting to note that the content of fat-soluble vitamins (vitamins A, D, E, K) in egg yolk strongly depends on the hen's diet . (see section 4.2 ). In addition to these vitamins, Eggs are an important source of choline, which is essentially concentrated in the yolk (680 mg/100 g in the yolk versus 1 mg/100 g in the egg white) [ 30 , 53 ]. In foods, choline is found in both water-soluble forms (free choline, phosphocholine, and glycerophosphocholine) and fat-soluble forms (phosphatidylcholine and sphingomyelin) and has important and diverse functions in both cell maintenance and growth throughout life. It plays roles in neurotransmission, brain development, and bone integrity. [ 54 , 56 , 57 ].
Egg vitamins (average content; µg/100g).
2.2.2. Minerals and trace elements
The egg is rich in phosphorus, calcium, potassium and contains moderate amounts of sodium (142 mg per 100 g of whole egg) ( Table 3 ). It also contains all the essential trace elements including copper, iron, magnesium, manganese, selenium and zinc ( Table 3 ), with egg yolk being the main contributor to the supply of iron and zinc. The presence of such minerals and micronutrients in eggs is quite interesting as a deficiency of some of them (Zn, Mg and Se) has been associated with depression and fatigue [ 59 ] and the development of pathological diseases. The concentration of some of these trace elements (selenium, iodine) can increase significantly depending on the diet of the hen (see paragraph 4.2 ).
Egg minerals and trace elements (average content; mg/100 g).
2.3. Antinutritional factors
As mentioned above, The main egg proteins include protease inhibitors that can delay the proper degradation of egg proteins by inhibiting digestive enzymes including pepsin, trypsin, and chymotrypsin. In fact, egg white is a major source of ovostatin, ovomucoid, ovoinhibitor, and cystatin [ 47 ]. Furthermore, some of these molecules (ovoinhibitor, ovomucoid, cystatin) possess many disulfide bonds which can confer moderate resistance to denaturation by proteases and gastric juices.
Some of these antinutritional factors can be partially denatured by heat [ 20 , 22 , 23 , 24 ] during the cooking process, thus facilitating the access of proteins to digestive proteases. In addition, some proteins that bind the highly concentrated vitamins in the egg can also limit access to vitamins: avidin that binds vitamin B12 (biotin) shows the highest known affinity in nature between a ligand and a protein [ 60 ].
The bioavailability of biotin to consumers may be compromised by the tight complex formed between avidin and its bound vitamin B8.
3. Egg-based nutraceuticals
There is growing evidence that the egg is not only a staple food with high nutritional value, but also contains many bioactive compounds (lipids, vitamins, proteins and derived hydrolytic peptides) [ 16 , 61 , 62 , 63 , 64 ] of great interest for human health. In vitro analyses performed on purified proteins have revealed great potential in egg proteins as they exhibit a diversity of biological activities. Various tools combining physicochemical, analytical and in silico approaches [ 65 , 66 ] can be used to identify hydrolytic peptides with potential bioactivities. It is remarkable that many egg proteins still have no identified physiological function, other than providing essential amino acids for the embryo but also for egg-feeding species, including humans. In addition to egg proteins showing a broad spectrum of antimicrobial activities that could contribute to gut health, many efforts have been made in the last decades to further characterize the biological activities of egg-derived hydrolytic peptides that may occur naturally during the digestive process [ 20 , 22 ]. Interestingly, some of these bioactive peptides are specifically generated after limited proteolysis of denatured egg proteins [ 67 ], after boiling. Most of these studies were conducted in vitro, but this finding opens up many fields of research. To date, little is known about how egg proteins resist the acidic pH of the stomach, digestive proteases and gut microbiota and how the presence of egg protease inhibitors in the diet may interfere with egg protein degradation by digestive proteases. The kinetics of protein digestion is sequential, starting with the hydrolysis of proteins into peptides until complete degradation into dipeptides and finally free amino acids. But It is known that some egg proteins (ovalbumin, ovomucoid) are only partially digested [ 20 , 22 ] suggesting that some bioactive peptides can be generated naturally without undergoing complete degradation into amino acids.
3.1. Antimicrobials
Egg antimicrobials in edible parts are mainly concentrated in the albumen and the vitelline membrane. Depending on the protein considered, these antimicrobials can exhibit antibacterial, antiviral, antifungal or antiparasitic activities ( Table 4 ).
Major antimicrobial proteins of the egg.
Their antibacterial effect is based on various bactericidal or bacteriostatic mechanisms.
Some of them have a potent activity through interaction with bacterial walls that further triggers permeabilization and bacterial death (lysozyme, avian beta-defensins, etc.). The effects of other molecules are rather indirect by decreasing the bioavailability of iron (ovotransferrin) and vitamins (avidin) necessary for some microbial growth and by inhibiting microbial proteases that are virulent factors of infection (ovoinhibitor, cystatin). [ 68 ] . The various egg antimicrobial molecules that have been described in the literature so far are listed in Table 4 . Interestingly, some of them (AvBD11, OVAX, avidin, beta-microseminoprotein) are not expressed in the human genome [ 69 ], suggesting that they could constitute potent anti-infective agents against human enteric pathogens, to strengthen the intestinal immunity of the host.
In addition to these egg proteins and peptides, there is increasing data reporting the antimicrobial activity of egg-derived peptides that can be released after partial hydrolysis by exogenous proteases. Such hydrolytic peptides obtained from lysozyme [ 70 , 71 , 72 , 73 ], ovotransferrin [ 25 ], ovomucin [ 74 ] and cystatin [ 75 ] have shown a wide range of antibacterial activities.
3.2. Antioxidant activities
Long-term oxidative stress in the gastrointestinal tract can lead to chronic intestinal disorders and there is growing interest in studying the potential of food-derived antioxidants, including egg antioxidants, in intestinal health. Chicken egg contains many antioxidant compounds including vitamins, carotenoids, minerals and trace elements but also the major egg white proteins [ 103 , 104 , 105 , 106 ] such as ovotransferrin, in its native form or as hydrolytic peptides [ 98 , 99 , 104 , 105 , 107 , 108 , 109 , 110 ], ovomucoid and ovomucoid hydrolysates [ 111 , 112 ], ovomucin hydrolysates and derived peptides [ 112 ] and egg yolk proteins including phosvitin [ 113 ]. Most of these molecules have been generated in vitro, but some assays performed on a porcine model revealed the beneficial effect of egg yolk-derived proteins in reducing the production of pro-inflammatory cytokines [ 114 ]. The authors concluded that dietary supplementation with egg yolk proteins may be a novel strategy to reduce intestinal oxidative stress [ 114 ].
3.3. Anti-Cancer Molecules
There are only a few data showing that food-derived proteins and peptides may also be useful in preventing and treating cancer diseases [ 26 ]. Several studies have confirmed the tumor-inhibiting activity of egg white lysozyme using experimental tumors. Its effect is essentially based on immunopotentiation [ 115 ]. Ovomucin (beta subunit) and ovomucin-derived peptides have also shown antitumor activities through cytotoxic effects and activation of the immune system [ 74 ]. The antitumor effect of egg tripeptides [ 27 ] and ovotransferrin hydrolytic peptides [ 116 ] have been published. Information in this field is rather scarce, but it may be worthwhile to continue investigating such activities. Some interesting data may come from studies on egg protease inhibitors [ 47 ] since similar molecules existing in other food products, including legumes such as peas, have been described as potential colorectal chemopreventive agents [ 117 ].
3.4. Immunomodulatory activities
Several egg proteins have potential immunomodulatory activities. Among them, egg white lysozyme is a promising agent for the treatment of inflammatory bowel disease. In a porcine colitis model, lysozyme was shown to significantly protect animals from colitis and reduce the local expression of pro-inflammatory cytokines while increasing the expression of anti-inflammatory mediators [ 118 ]. Sulfated glycopeptides generated by proteolysis from ovomucin, chalazae, and yolk membrane can exhibit macrophage-stimulating activity in vitro [ 74 ]. Cytokines, such as egg white pleiotropin, play a critical role in the generation and resolution of inflammatory responses. In humans, pleiotropin has been shown to promote lymphocyte survival and drive immune cell chemotaxis. 119 , 120 ]. But the biological significance of the potential immunomodulatory activity of egg white pleiotropin in the human intestine remains highly speculative. On the contrary, some valuable immunomodulatory activity might emerge from ovotransferrin and vitellogenin hydrolysates of egg yolk [ 121 , 122 ] after partial degradation by digestive proteases.
3.5. Antihypertensive activity
Considering the prevalence and importance of hypertension worldwide (over 1.2 billion individuals) [ 123 ], there is an increasing research to find ways to regulate this multifactorial disease. At the population level, the most important factors for long-term blood pressure control are sodium and potassium intake and the importance of the renin-angiotensin-aldosterone system. Most egg-derived peptides with antihypertensive activity exhibit inhibitory activities against angiotensin-converting enzyme (ACE). This enzyme triggers the processing and activation of angiotensin I into the active vasoconstrictor angiotensin II. Several egg yolk-derived peptides with antihypertensive activity have been described in the literature [ 113 , 124 ] along with ovotransferrin and egg white hydrolysates [ 125 , 126 ]. Some of these peptides contain only three amino acids [ 27 , 127 ]. Some of these tripeptides have been shown to be active in vivo: oral administration of these peptides that were administered orally to hypertensive rats helped to significantly reduce blood pressure [ 128 ] and thus may help to reduce the occurrence of cardiovascular disease [ 127 , 129 ].
4. Factors that influence egg quality
4.1. Genetics
Selection for egg quality is an important component of the breeding strategies of companies marketing laying hens. In fact, consumers demand high-quality products with a robust eggshell, reducing costs, ensuring eggs free from microbial contaminants and improving the acceptability of farming systems [ 130 , 131 ].
Most breeding strategies to improve egg quality have focused on the physical properties of the shell (and its ability to resist impacts), egg weight stability, albumen quality and yolk percentage. Albumen quality essentially refers to the height of the albumen which reflects freshness and its ability to prevent microbial growth and survival that may be associated with toxin infection risks for consumers (salmonellosis). Recently, some authors reported differences in albumen height/pH in various selected lines [ 132 ] and confirmed that selection on specific traits modified the proportion of yolk, albumen and shell by increasing albumen height. Moderately high variability in egg yolk and albumen weights was also observed when comparing selected and traditional lines [ 133 ]. Egg white is a very unfavorable medium for bacteria, due to its high viscosity, its pH which becomes progressively alkaline during egg storage (from 7.8 to 9.5) and the presence of a myriad of antimicrobial molecules (see section 3.1 ). Indeed, it has been shown that the antibacterial potential of egg white is moderately heritable [ 134 ]. As for egg proteins and peptides, Some differences in the relative abundance of some molecules have been reported in brown versus white eggs or in different lines , but the major egg proteins remain essentially unchanged [ 135 , 136 ].
4.2. Feeding and breeding systems
The diet of laying hens, feed characteristics (nutrient composition, energy content, but also feed texture and presentation) and the way feed is delivered during the day influence not only egg weight, but also to a lesser extent the egg-yolk to albumen ratio [ 137 ]. The quality of the pullet diet will influence egg weight essentially at the beginning of laying , but is much less significant when considering the entire laying period [ 137 ]. Dietary characteristics include the level of calcium intake and its particular size. Dietary calcium in a particular form allows hens to express a specific appetite for calcium at the end of the day, which is stored and further assimilated during the night when eggshell formation occurs [ 138 ]. Egg weight is influenced by the daily energy consumption of hens. High energy diet and dietary linoleic acid intake increase egg weight. This effect is particularly significant at the beginning of laying (22–32 weeks) and much less pronounced in older hens. [ 139 ].
Egg weight is also increased by the level of dietary protein and some studies have revealed that Methionine was the major limiting amino acid since its presence in the hen's diet is positively correlated with egg weight [ 140 ]. Furthermore, energy intake depends on the protein source, considering that Laying hens are traditionally fed with corn, wheat and soybean meal. The presence of antinutritional factors in the diet (protease inhibitors and proteins highly resistant to digestive proteases such as convicilin, glycinin, cruciferine [ 141 ]) can influence the overall digestibility of the feed by the hens and the resulting egg weight. However, the content in the main components of the egg is relatively stable and the variability depends essentially on the proportion of albumen to yolk, which show a very contrasting composition (see section 2 ).
In contrast, the fatty acid profile of the yolk and the content of micronutrients such as vitamins and trace minerals (see section 2.2 ) or carotenoids are highly variable and directly depend on the composition of the diet [ 137 ].
The fatty acid profile of an egg, incorporated into triglycerides and phospholipids, directly reflects the fatty acid composition of the hen's diet.
In contrast, enrichment of the hen's diet with saturated fatty acids has a lesser influence on the lipid profile of the yolk. The content of saturated and unsaturated fatty acids in the hen's diet can be modified by the inclusion of oil or feeds that show a high degree of unsaturated fatty acids such as fish, chia, flax seeds [ 142 , 143 ], olive oils or soybean (see Reference [ 144 ] for a review). For example, including olive oil in a hen's diet promotes the incorporation of monounsaturated fatty acids (particularly oleic acid content) into the yolk, while soybean oil increases that of n-6 unsaturated fatty acids (linoleic acid) [ 144 ].
More recently, results obtained with a dietary enrichment with microalgae or flaxseed have revealed the potential of these compounds to increase the yolk content of n-3 fatty acids (more than 3- and 4-fold increase, respectively) [ 145 ] . A similar trend of increasing polyunsaturated content of yolk was observed with powdered calendula extract [ 146 ], the microalgae Schizochytrium [ 147 ], the combination of prebiotics and probiotics [ 148 ] ], etc.
According to Rocca et al. [ 24 ] Chicken eggs can be beneficially modified by camelina seed oil ( Camelina sativa (L.) Crantz), which is rich in omega-3 essential fatty acids, resulting in functional eggs that have positive effects on human health. Camelina is an oilseed belonging to the Brassicaceae family [ 25 ].
Eggs can, therefore, represent an alternative to fish and oilseeds, both as a source of omega-3 fatty acids [ 24 ] and from an economic point of view due to the low price of table eggs. [ 29 ]. Furthermore, the introduction of egg variants (such as eggs enriched with omega-3 fatty acids) on the market should represent an attractive alternative given the growing consumer demand for healthy and safe foods [ 30 ].
In conclusion, it is relatively easy to enrich the egg in some unsaturated fatty acids, of interest for human health. The challenge remains to identify animal and plant sources of polyunsaturated fatty acids that increase the content of these fatty acids in the yolk without affecting its technological and/or sensorial quality, to meet both the needs of the food industry (egg products) and consumer demand.
The content of some trace minerals in eggs such as selenium, iodine and, in smaller amounts, iron, zinc, fluoride or magnesium can also be increased by increased dietary intake for hens [ 149 ]. The average selenium content is about 5 µg per egg and can be increased 3- to 6-fold (12-fold in the albumen and 4-fold in the yolk) and reach 30–40 µg/egg when hens are supplied with 0.3 to 0.5 mg selenium (from selenomethionine yeast or selenium-enriched/kg diet). Such egg enrichment provides 50–70% of the daily human requirement [ 150 ].
Similarly, hen feeding is a way to enrich the egg with fat-soluble vitamins (A, D, E, K) or water-soluble vitamins (folate, B12, pantothenic acid and, in smaller quantities, riboflavin, thiamine and biotin). The vitamin A content of eggs can be increased 10-fold compared to its initial value when hens receive 30,000 IU of retinol and that of vitamin D3 15-fold (from 2–5 to 34 µg/100 g in hens fed 2500 and 15,000 IU D3). The vitamin E content in the yolk can increase 3-20 times depending on the content of the basal diet and the feed intake. For water-soluble vitamins, the extent of increase due to increased dietary intake is lower, more than 2-fold for folate, riboflavin or cobalamin and, to a lesser extent, thiamine, biotin and pantothenic acid, pyridoxine or niacin [ 137 ]. The colour of the yolk (yellow/orange tinge) is also determined by the carotenoid content in the diet [ 137 ]. The main sources of carotenoids (lutein, xanthophylls and zeaxanthin) for birds are corn, alfalfa, flower (marigold) and paprika extract (red carotenoids) which are incorporated into a hen's diet to meet consumer demand for a more yellow-orange yolk . In addition to its interest in increasing the visual appearance of the yolk, the high carotenoid content in the yolk may also have a positive impact on human health in increasing visual performance and reducing the risk of age-related macular degeneration [ 151 ].
Since birds in free-range systems have access to grass, insects and worms in addition to their basic diet, the content of some micronutrients in eggs may also vary slightly. For example, Free-range systems result in significantly higher total tocopherol, alpha-tocopherol and lutein content , compared to battery cage and organic systems, respectively, when hens are fed a similar conventional diet [ 152 ]. In contrast, no significant differences were observed in lipid and total sterol content [ 152 ]. A decrease in albumen height and yolk color was also observed when comparing eggs from conventional cages with free-range systems [ 153 ]. However, eggs from conventional systems contain, in general, more carotenoids and vitamins due to the possibility of including chemical additives in the diet, knowing that such a practice is not conducted in organic systems . In parallel, since the immune system of hens is likely to be more challenged by the presence of environmental microbes in free-range systems, an increase in the content of immunoglobulin Y in egg yolk (initially to provide some passive immunity to the chick, similar to maternal colostrum for babies) is likely to increase. Furthermore, Some have shown that the antimicrobial capacity of egg white can even be slightly modulated when hens are exposed to environmental microbes. [ 154 ]. In conclusion, raising laying hens in free-range systems can globally improve the antimicrobial potential of eggs. (see section 3.1 ).
4.3. Physiological state
Egg production and quality are strongly influenced by the physiological state of the hen: age, stress and immune status [ 155 ]. Egg weight ranges from 50 g to 70 g, depending mainly on the age and genetics of the hen (see Section 4.1 ). In the modern flock, egg weight has been limited to 62–66 g throughout the laying cycle (20 to 80 weeks of age). Egg weight is the main criterion used in classifying eggs (small, medium, large, extra-large). The increase in egg weight observed in older hens is associated with an increase in the mean weight of albumen and yolk and the relative proportion of yolk [ 156 ]. Hen age is also associated with a decrease in eggshell strength, albumen height (the higher the albumen height, the higher the degree of freshness) [ 153 ] and a decrease in vitelline membrane strength which is often associated with an increased incidence of yolk breakage [ 157 ]. It is likely that this latter observation results from an increase in the proportion of yolk in older hens. However, when considering the chemical composition of eggs, the results are rather controversial, although some have shown some differences in the fatty acid composition (docosahexaenoic acid and arachidonic acid) of eggs depending on the age of the hen [ 158 ]. Overall, these alterations in egg quality with age are, however, consistent with physiological changes and perhaps some primary metabolic dysfunctions that occur in commercial hens at the end of the laying cycle [ 159 ].
Egg-laying performance also depends on the general health of the hen as diseases and infections can induce loss of appetite and physiological failure thus affecting the growth of the animals, egg laying and egg quality (eggshell deformation, eggshell defects, albumen thinning, etc.). The most commonly found microbes in laying hens that affect the hygienic quality of eggs are Salmonella enterica Enteritidis, Mycoplasma, Infectious bronchitis virus and Avian influenza virus [ 160 ]. Another major problem for hen welfare and egg quality is the poultry red mite which is found in most laying hen systems, regardless of the type of system [ 161 ]. As a blood feeder, this mite has dramatic effects on the welfare of the chicken host, including distress, anemia, reduced egg production and reduced egg quality. [ 162 ]. The prevalence of red mites is expected to increase, following recent changes in legislation on chicken farming (in favour of cage-free systems), increasing resistance to acaricides, global warming and the absence of efficient and sustainable solutions to control infestations [ 163 ]. It is also a major public health concern as it could be a vector of food-borne pathogens, including Salmonella species [ 164 ]. Among all these microbes, Salmonella enterica Enteritidis is the most critical for egg consumers as this pathogen can survive in egg white [ 165 ], even after several weeks of storage at 4 °C and 25 °C [ 166 ] and be responsible for food-borne diseases. It remains the dominant pathogen associated with egg consumption [ 167 ]; however, authorities have made considerable efforts to control the spread of Salmonella Enteritidis along the egg production chain. The number of reported salmonellosis cases has continued to decline due to the implementation of effective Salmonella control programmes in poultry production [ 168 ], including detection and monitoring of Salmonella [ 169 ], the adoption of pre-harvest measures [ 170 ], management and sanitation measures [ 171 ], and decontamination of eggs by washing under certain conditions [ 172 ].
Interestingly, European legislation does not allow egg washing in Europe (Commission Regulation (EC) No 589/2008), “because potential damage to physical barriers, such as the cuticle, may promote trans-shell contamination with bacteria and moisture loss and thus increase the risk to consumers, particularly if subsequent drying and storage conditions are not optimal”.
4.4. Egg storage and heat treatment
Shell eggs are stored at room temperature or preferably in the refrigerator before being used by consumers ( eggs are considered “fresh” up to 28 days after laying ). Storage conditions of eggs can induce profound internal changes including physicochemical changes that can increase some technological properties useful for the food industry and the alteration of the antibacterial properties of the albumen [ 173 , 174 , 175 , 176 ] ( Figure 3 ). These alterations result from the exchange of water between yolk and albumen and from the loss of water and carbon dioxide through the pores of the eggshell, which resulted in an increase of the air cell developing between the two membranes of the eggshell ( Figure 3 a). The height of the albumen decreases with storage time while the pH of the albumen and the churning volume increase [ 136 ]. In parallel, the strength of the vitelline membrane decreases during egg storage due to loosening, thus influencing the shape/index of the yolk (the yolk becomes flat and its diameter is higher) [ 173 ]. These latter modifications favor egg white/yolk exchanges of components such as carbohydrates and glucose [ 177 ], proteins [ 178 , 179 , 180 ], vitamins and trace elements [ 181 ]. Furthermore, storage duration and conditions are associated with protein degradation [ 175 , 179 , 180 ] and a decrease in its antibacterial potential [ 175 ]. However, except for proteins, only little information is available describing the changes/denaturation of lipids, vitamins and minerals composing both egg white and egg yolk during storage. It will be interesting to further study how these modifications affect the respective functional, nutritional and technological properties of egg yolk and egg white (foaming properties, emulsifying properties, etc.).
Recent data have shown that the antioxidant activity of egg yolk remained globally unchanged during six weeks of retail storage [ 182 ]. All these alterations in freshness criteria are accelerated at room temperature compared to refrigerated conditions.
In addition to storage, it would be expected that egg nutrients may also be altered during cooking. No clear evidence of denaturation of minerals or vitamins can be observed when comparing fresh, soft-boiled and hard-boiled eggs ( Table 5 ).
List of egg characteristics and main components that vary during cooking.
In fact, some data appear contradictory from one reference source to another (CIQUAL vs. USDA, Table 5 ). In any case, It appears that the amount of polyunsaturated fatty acids, selenium and vitamin A [ 21 ] tends to decrease during cooking , especially in hard boiled eggs ( Table 5 ).
In particular, Proteins undergo significant conformational changes during cooking, although their relative amount is not affected by cooking ( Table 5 ). This protein denaturation may be useful to inactivate antinutritional factors such as egg white antiproteases, but also to denature highly resistant proteins, thus facilitating protease activity in the digestive tract. Increased digestibility of egg proteins may also help to limit egg hypersensitivity in children [ 183 , 184 ]. In the meantime, Cooking has been shown to significantly reduce the oxygen radical scavenging capacity (antioxidant potential) of egg yolk associated with free aromatic amino acids, lutein and zeaxanthin [ 182 ] and also affects yolk lipids [ 185 ] ]. These observations confirm that taking into account the food matrix and the way in which eggs are prepared is of fundamental importance to appreciate the digestibility of eggs and the associated nutritional and nutraceutical quality. [ 186 ]. To conclude, it is quite difficult to assess the risk/benefit ratio of cooking eggs for human health since many molecules can be affected by cooking, while, in parallel, the heating process can increase the digestibility of egg proteins and potentially reveal potential new bioactive peptides [ 187 , 188 ]; but It is worth remembering that cooking eggs also allows the elimination of potential pathogens responsible for toxic infections in consumers. In conclusion, taking into account all these data, the advice to preserve most of the nutritional and nutraceutical benefits associated with the egg would be to favor the consumption of poached or soft-boiled eggs, where the egg white is cooked (to inactivate antinutritional factors and potential bacterial pathogens) while the egg yolk remains essentially raw (to preserve most of the vitamins, lipids, micronutrients and some bioactive molecules (antioxidants).
4.5. Variability among domestic avian species
The table egg market is dominated by chicken eggs in all countries. However, duck eggs are also widely consumed in some Asian countries. The main reason for this rise of chicken eggs is based on several reasons: Chickens are easy to handle and raise and have been bred for decades to lay nearly 320 eggs per year . In contrast, geese, turkeys and ducks are seasonal layers and require more specific sanitary and husbandry conditions. Chicken eggs are also reasonably sized, not too large and larger than quail eggs, the latter occasionally eaten as a gourmet ingredient.
Although egg compositions of traditional domestic species share common characteristics [ 189 , 190 ], they possess some significant differences in energy that are mostly explained by the change in the relative proportion of yolk to egg white ( Figure 4 ). The energy (kcal/100 g) for chicken, quail, duck, goose and turkey eggs is 143, 158, 185, 171, respectively. While the relative amount of protein remains stable across species (about 13%), the lipid proportion varies from 9.5% (chicken) to over 13% (duck, goose) ( Figure 4 , which explains most of the variation in the respective energy value. The yolks of duck and goose species have a relatively higher fat content and a higher yolk percentage than the chicken egg [ 189 ]. In parallel, the lipid profile of egg yolk shows some species-specific specificities [ 191 , 192 , 193 ]. Overall, the composition of duck egg resembles that of goose egg, which is consistent with their phylogenetic closeness.
It is also interesting to note that the mineral and trace element content of chicken eggs is generally lower than that observed for other species, particularly in duck and goose species. ( Table 6 ). A similar trend is observed for vitamins ( Figure 5 ). However, it should be noted that the variation of vitamins and trace elements in eggs depends mainly on the composition of the diet. Therefore, these differences may reflect the conditions of breeding the birds rather than the genetic ability of the hens to retain these compounds in the eggs.
Comparison of egg minerals and trace elements in chicken, quail, duck, goose and turkey eggs (average content; mg/100 g).
In addition to these chemical compounds, some variability in bioactive molecules has also been reported. Indeed, comparative analysis of egg white and egg yolk proteomes has revealed some proteins that are specifically associated with one or the other species [ 194 , 195 , 196 , 197 ] and others (ovotransferrin, lysozyme, hen), which show differences in abundance [ 196 ]. Overall, these characteristics may influence the overall bioactive potential of the albumen extract (antibacterial and/or antioxidant activity) depending on its bird origin, and It has been shown that chicken egg white retains the highest antibacterial potential compared to turkey, duck and goose egg white, at least against some bacterial strains (Bacillus subtilis, Staphylococcus aureus, Pseudomonas aeruginosa and Escherichia coli) [ 91 ]. Furthermore, The lower abundance of ovomucoid (a protease inhibitor highly resistant to chemical and thermal denaturation) in duck, goose or turkey egg white [ 196 ] may be associated with higher protein digestibility.
In conclusion, it is likely that such differences in the chemical composition of the egg, and also in some of its biologically active molecules, are correlated with an increased or lower nutraceutical value of some egg proteins of other species, compared to the hen egg.
5. Conclusions
For centuries, eggs have been considered a food with high nutritional value for humans and are widely consumed worldwide. Its consumption is expected to continuously increase in the future, considering the increasing number of Western consumers who start adopting a meat-free diet (vegetarians) or significantly reduce their meat consumption. This change in our consumption patterns and eating habits is motivated by many data on the association of the risk of meat intake with digestive cancers and cardiovascular diseases and by a growing number of studies praising the vegetarian diet [ 198 , 199 , 200 , 201 ]. In parallel, it is also driven by ethical and environmental concerns regarding the ways of meat production [ 202 ]. It should also be highlighted that there are substantial disparities in egg consumption between countries [ 18 ], which is particularly low in Central Africa, with only 36 eggs/year/capita [ 19 ]. The development of the egg industry in developing countries can represent a great opportunity for human nutrition/health and economy.
In addition to basic nutrients, eggs are also an excellent source of potential nutraceuticals.
A total of 550 distinct proteins have been identified in the albumen and yolk/vitelline membranes to date, and the physiological function of only 20 of them has been characterized so far. This observation suggests that the egg probably still harbors many unknown activities that deserve further investigation considering the current lack of research evaluating the fate of egg proteins along the digestive tract. Such studies could help to better appreciate the in vivo potential of egg proteins and the resulting hydrolytic peptides and could be easily learned using dynamic gastric models that have been used with other foods, in food and pharmaceutical research [ 203 , 204 ]. These in vitro models mimic both the biochemical and mechanical aspects of gastric digestion. They incorporate artificial saliva, compressive forces to disintegrate the food, simulate continuous gastric emptying and gastric secretion that generate pH profiles similar to the human stomach. They also include bile salts and intestinal enzymes that act sequentially in a realistic and time-dependent manner [ 205 ] and can be improved by adding gut-like microbiota. This model has already been used in a wide range of studies to assess the bioaccessibility of nutrients and to study structural changes in food matrices. It is expected that such an experimental strategy would be a promising way to study the impact of dietary egg preparation (raw or cooked) on the physiological generation of bioactive peptides and to better appreciate their biological significance for human health. It is now assumed that gut health depends on the interplay between the host genome, nutrition and lifestyle that contributes to normal brain function and mental health [ 206 ].
Sources:
- Nutrients. 2019 Mar; 11(3): 684. doi: 10.3390/nu11030684
- The Golden Egg: Nutritional Value, Bioactivities, and Emerging Benefits for Human Health
