Introduction
The main characteristics of commercial egg production in industrial systems include confinement facilities, artificial lighting and ventilation, a large number of highly productive hybrid layers kept in limited space (mostly in battery cages), intensive feeding, and use of many hygiene and maintenance products. These factors have contributed to battery farming becoming the most common table egg production system in the world (Matt et al., Reference MATT, REMBIALKOWSKA, LUIK, PEETSMANN and PEHME2011).
More recently, alternative laying hen rearing systems have been introduced to harmonise poultry health and welfare with consumer, producer, industry and environmental demands (Matković et al., Reference MATKOVIĆ, VUČEMILO and MATKOVIĆ2007). The most common alternative laying hen rearing systems include free run, free range, pastured, organic and omega 3 (Henry, Reference HENRY2002). Non-scientific circles often do not distinguish between free range and organic rearing systems, since both include the use of outdoor access, but there is a difference between them, as organic poultry has specific housing requirements and must be kept in a free range system and fed only organic feed. Laying hens must have free access to the outdoors. Organic egg producers cannot use antibiotics except during an infectious outbreak (Matt et al., Reference MATT, REMBIALKOWSKA, LUIK, PEETSMANN and PEHME2011). Fanatico (Reference FANATICO2007) described organic production system as a pasture-based system and, if the producer chooses to follow the certification process, which requires that feed, pasture and processors be certified organic. In terms of organic production, the USDA's National Organic Program requires outdoor access and organic feeds produced without synthetic chemicals, and prohibits the use of antibiotics. Although the poultry digestive system cannot convert plant-based fibres into energy as efficiently as the digestive system of ruminants (Burbaugh et al., Reference BURBAUGH, TORO and GERNAT2010), this intake can increase the quality of poultry meat and eggs (Karsten et al., Reference KARSTEN, PATTERSON, STOUT and CREWS2010), with the animal products obtained being more nutritional and more suitable to human health (Ishibashi and Yonemochi, Reference ISHIBASHI and YONEMOCHI2003; Kouba, Reference KOUBA2003; Rembiałkowska and Średnicka, Reference REMBIAŁKOWSKA and ŚREDNICKA2009).
Significant amounts of table eggs from these alternative systems are already available to certain countries (as much as 23% of eggs that reach the Danish market come from hens that have access to the outdoors according to Hegelund et al., Reference HEGELUND, SORENSEN and HERMANSEN2006). In the USA, organic egg sales have had annual growth rates of 20% since the 1990s, thus making the organic egg market the fastest growing part of the organic agriculture sector (Oberholtzer et al., Reference OBERHOLTZER, GREENE and LOPEZ2006). This is further illustrated by the information that 15% of consumers in the USA purchase organic eggs (Hilmire, Reference HILMIRE2012).
Free range systems use hybrids or indigenous breeds adapted to existing environmental conditions. The hen breed used is often dependent on the colour of eggs laid. White Leghorns are among the most popular and productive layers of white eggs whereas Rhode Island Reds are the second most popular and produce large brown eggs in the USA (Burbaugh et al., Reference BURBAUGH, TORO and GERNAT2010), whereas Hilmire (Reference HILMIRE2012) mentioned Plymouth Rocks and Ameraucanas breeds as largely used for the production of brown-shelled eggs. Ishibashi and Yonemochi (Reference ISHIBASHI and YONEMOCHI2003) reported that as much as 70% of Japanese consumers consider brown-shelled eggs more preferable, more nutritious and flavoursome as compared to white-coloured eggs.
Proteins
The high content of highly bioavailable protein in eggs is of great benefit to human nutrition (Anton, Reference ANTON2007). Minelli et al. (Reference MINELLI, SIRRI, FOLEGATTI, MELUZZI and FRANCHINI2007) found a higher protein level in the yolks of eggs from organic Hy-Line Brown birds (17.1%) than in cage-kept laying hens (16.7%). Hidalgo et al. (Reference HIDALGO, ROSSI, CLERICI and RATTI2008) showed a significantly higher protein content in the whole egg in each of the alternative rearing systems employed viz free range (12.5%), barn (12.6%) and organic (12.5%), as compared to conventional cage system (12.1%). Kucukyilmaz et al. (Reference KUCUKYILMAZ, BOZKURT, HERKEN, CINAR, CATH, BINTAS and COVEN2012) reported a higher protein level in the whole egg from organic Lohmann LSL birds (13.19%) than in caged laying hens (12.85%). Interestingly, no difference was found in egg protein level between ATAK-S birds reared under organic or cage systems in the same experiment, indicating that rearing system does not necessarily lead to changes in the egg protein content. This was confirmed by Rizzi et al. (Reference RIZZI, SIMIOLI, MARTELLI, PAGANELLI and SARDI2006) who found no difference in egg protein level between caged and free range Isa Brown birds.
On the other hand, Pavlovski et al. (Reference PAVLOVSKI, ŠKRBIĆ, LUKIĆ, LILIĆ, KRNJAJA, STANIŠIĆ and PETRIČEVIĆ2011) obtained a higher protein percentage in the eggs of Hy-Line Brown hens kept in cages (12.34%) than under a free range environment (11.93%). Similar results were reported by Matt et al. (Reference MATT, VEROMANN and LUIK2009), who found a higher protein level in the same hybrid in caged birds (12.35%) than in organic layers (11.90%). Furthermore, Krawczyk (Reference KRAWCZYK2009) measured a higher protein content in the albumen in Greenleg partridge chicken breed reared under conventional systems (10.6%) than under organic system (10.3%), whereas the highest values were obtained in eggs from backyard systems, with the average protein content of the egg white of 11.7%.
Lysozyme, ovomucoid, ovoinhibitor and cystatin are biologically active proteins in egg albumen, protecting the embryo during the incubation period, and their activity prolongs the shelf life of table eggs. Cystatin, as a substance with high inhibitory activity against cysteine proteases, has antibacterial and antiviral qualities and is a factor inhibiting the development of cancer cells (Wesierska et al., Reference WESIERSKA, SALEH, TRZISZKA, KOPEC, SIEWINSKI and KORZEKWA2005). Activities of these biological substances in egg albumen are affected by conditions and management systems (intensive, extensive) of laying hens (Trziszka et al., Reference TRZISZKA, KOPEĆ, SKIBA and DOBRZAŃSKI2006). The same authors, in an experiment with two hybrids (Lohmann and Tetra) under three rearing systems (battery, litter and free range), determined lysozyme content ranging from 1073 to 1235 (in 2.5 mg protein), but it depended more on the breed of layers than on the production system. Significant differences were observed between Lohmann and Tetra layers, whereby the lysozyme level from Tetra layers was similar in both the battery and free range systems. The level of cystatin indicated that eggs obtained from layers kept in battery and free range system showed similar activity (ca. 21 units/5 mg protein), while keeping hens on litter led to very low activity. The highest antitrypsin activity of the egg white was observed in eggs collected from hens kept in cages (battery system, Tetra hybrid), whereas eggs derived from hens housed in more ecological systems (free range and on litter) were characterised by slightly lower activity of ovomucoid. Trziszka et al. (Reference TRZISZKA, DOBRZAŃSKI, SKIBA and KOPEĆ2007) found the highest activity of lysozyme (116.12 units per 100 mg of protein) in eggs from Lohmann Brown layers kept in a battery system, and lower values in free range laying hens (100.59 units per 100 mg of protein) and birds kept on litter (98.20 units per 100 mg of protein). Cystatin activity was highest in birds reared on litter (4.237 units per 1000 mg of protein), followed by battery birds (2.623 units per 1000 mg of protein), and the lowest levels in free range layers (1.483 units per 1000 mg of protein).
In contrast, Swierczewska et al. (Reference SWIERCZEWSKA, SKIBA, SOKOLOWSKA, NOWORYTA-GLOWACKA, KOPEC, KORZENIOWSKA and BOBAK2005) found that the hens managed in an extensive type of housing system laid eggs with a higher activity of lysozyme, cystatin, ovoinhibitor and ovomucoid, as compared to eggs originating from the layers kept in an intensive housing system.
Lipids
Lipids are the main components of fresh yolk (about 30%). Yolk lipids are exclusively associated with lipoprotein assemblies. They are made up of 62% triglycerides, 33% phospholipids, and less than 5% cholesterol. Carotenoids account for less than 1% of yolk lipids, and they give it its colour (Anton, Reference ANTON2007). Egg yolk lipids are an important source of fat for humans (Pintea et al., Reference PINTEA, DULF, BUNEA, MATEA and ANDREI2012).
Cherian et al. (Reference CHERIAN, HOLSONBAKE and GOEGER2002) found differences in the lipid content of yolk, in their analysis of 6 types of eggs: ‘animal fat free-high n-3’ (SP1), ‘free range organic brown eggs’ (SP2), ‘uncaged- non-medicated brown eggs’ (SP3), ‘vegetarian diet cage-free brown eggs,’ (SP4) or ‘cage-free naturally nested no steroids no stimulants’ (SP5). Regular white-shelled eggs were used as the control. The lipid content in yolk was as follows: control 25.1%; SP1 27.7%; SP2 24.6%; SP3 26.2%; SP4 22.9% and SP5 25.9%.
Pintea et al. (Reference PINTEA, DULF, BUNEA, MATEA and ANDREI2012) compared two genotypes (Araucana and Isa Brown) in a free range system and found that the total egg yolk lipid content was significantly higher in the Araucana (27%) than in the ISA Brown eggs (20%). Matt et al. (Reference MATT, VEROMANN and LUIK2009) reported that Hy-Line layers had significantly higher lipid content in whole eggs from birds reared in conventional cages (8.88%) than in free range layers (7.94%).
In contrast, Samman et al. (Reference SAMMAN, KUNG, CARTER, FOSTER, AHMAD, PHUYAL and PETOCZ2009) found higher lipid percentage in whole eggs from floor-reared birds (4.46%) and free range hens (4.47%) than in those from caged layers (4.11%). Anderson (Reference ANDERSON2010) measured a higher lipid content in eggs from free range birds, whereas Tolan et al. (Reference TOLAN, ROBERTSON, ORTON, HEAD, CHRISTIEAND and MILLBURN1974), Cerolini et al. (Reference CEROLINI, ZANIBONI and LA COGNATA2005), Rizzi et al. (Reference RIZZI, SIMIOLI, MARTELLI, PAGANELLI and SARDI2006), Minelli et al. (Reference MINELLI, SIRRI, FOLEGATTI, MELUZZI and FRANCHINI2007), Hidalgo et al. (Reference HIDALGO, ROSSI, CLERICI and RATTI2008), Karsten et al. (Reference KARSTEN, PATTERSON, STOUT and CREWS2010), and Pavlovski et al. (Reference PAVLOVSKI, ŠKRBIĆ, LUKIĆ, LILIĆ, KRNJAJA, STANIŠIĆ and PETRIČEVIĆ2011) found no effect of rearing system on egg lipid percentage.
Vitamins
Vitamin concentration is influenced by genetics, egg production rate and hen diet composition (Leeson and Caston, Reference LEESON and CASTON2003). Eggs are recognised as a major source of vitamins in the diet (Matt et al., Reference MATT, REMBIALKOWSKA, LUIK, PEETSMANN and PEHME2011). Feed obtained from the pasture range have more vitamins (Mattocks, Reference MATTOCKS2002); hence, their egg content increases, since the two traits are mutually dependent (Sirri and Barroeta, Reference SIRRI and BARROETA2007). Under free range systems the chemical composition of eggs has been altered to meet consumer demands for increased colour intensity, vitamins and unsaturated fatty acids (Egerer and Grashorn, Reference EGERER and GRASHORN2008). Eggs from free-range hens have higher α-tocopherol and α-linolenic acid content when compared with eggs from hens fed a commercial mixed diet (Lopez-Bote et al., Reference LOPEZ-BOTE, SANZ ARIAS, REY, CASTANO, ISABEL and THOS1998). Krawczyk (Reference KRAWCZYK2009) compared vitamin content in Greenleg partridge chickens (a Polish indigenous breed) reared under organic, backyard and conventional systems. Vitamin A content in the three systems was 5.8, 6.3 and 5.1 ug/g respectively, and vitamin E content was 91.33, 36.42 and 84.05 ug/g, respectively. The differences were statistically confirmed. Lopez-Bote et al. (Reference LOPEZ-BOTE, SANZ ARIAS, REY, CASTANO, ISABEL and THOS1998) found α-tocopherol level to be significantly higher in free range Comb White Leghorn layers (86.22 ug/g yolk) than in conventional birds of the same hybrid (65.58 ug/g yolk). Mugnai et al. (Reference MUGNAI, DAL BOSCO and CASTELLINI2009) found statistically significantly higher α-tocopherol content in the eggs of Ancona laying hens from an organic plus system, as compared to organic and conventional systems. Matt et al. (Reference MATT, VEROMANN and LUIK2009) reported a higher content of vitamin A (0.57 mg/100 g), α-tocopherol (14.90 mg/100 g) and vitamin D (0.014 mg/100 g) in the eggs of Hy-Line Brown layers reared under organic system vs. conventionally reared birds of the same hybrid (Vitamin A-0.46, α-tocopherol-6.90, vitamin D-0.008 mg/100 g yolk).
Certain studies observed even more drastic differences in the content of liposoluble vitamins in the eggs of layers reared on free range and in cages, with the results from 14 organic farms showing four times more vitamin E and two times more vitamin A in free range eggs than in conventionally produced eggs (http://www.motherearthnews.com/eggs.aspx). Long and Alterman (Reference LONG and ALTERMAN2007) showed that free range hens produced eggs with two-thirds more vitamin A and three times more vitamin E compared to eggs from caged hens.
Karsten et al. (Reference KARSTEN, PATTERSON, STOUT and CREWS2010) evaluated the effect of different plants growing on the range on the nutritional quality of eggs, and found 38% more vitamin A and two times more vitamin E in free range birds than in conventionally reared caged layers. Moreover, vitamin E content was significantly higher in the eggs from hens reared on a grass-dominant range than in those from birds reared on a legume-dominant range. These results serve as another confirmation of the fact that the type of feed available on the range has a crucial effect on the content of liposoluble vitamins in the egg.
However, Anderson (Reference ANDERSON2010) reported no differences in vitamin A and vitamin E content in eggs from Hy-Line Brown layers raised free range or in cage system. Furthermore, it was observed that the egg vitamin content decreased with increasing age of layers.
Cholesterol
Cholesterol in eggs plays an important role in the development of the embryo. It is a structural component of cell membranes and precursor for hormones, vitamin D, and bile acids (Anton, Reference ANTON2007). Cholesterol concentration in eggs depends on the breed and age of layers, management and nutrition, and partly on synthesis in the liver (Matt et al., Reference MATT, VEROMANN and LUIK2009). The same authors found about 30% higher cholesterol levels (489mg/100g) in Hy-Line Brown eggs from organic systems compared to conventional hens (341mg/100g). In an experiment with the same hybrid, Minelli et al. (Reference MINELLI, SIRRI, FOLEGATTI, MELUZZI and FRANCHINI2007) obtained a higher cholesterol level in egg yolks of organic birds (1.26%) than in those of caged layers (1.21%).
Free range eggs may contain two-thirds more cholesterol compared to cage-raised birds (http://www.motherearthnews.com/eggs.aspx). A similar finding was reported by Kilikides (Reference KILIKIDES1970). Despite the reported increase in egg cholesterol content induced by free ranging, this need not be considered a negative consequence of this type of layer rearing, in view of the fact that Hu et al. (Reference HU, STAMPFER, MANSON, RIMM, WOLK, COLTIDZ, HENNEKENS and WILLET1999) reported that cholesterol from eggs does not have a negative effect on serum cholesterol levels and that there is no significant relationship between dietary cholesterol intake from eggs and coronary heart disease incidence.
In contrast to the above results, Long and Alterman (Reference LONG and ALTERMAN2007) showed that free-range hens produce eggs with about one-third less cholesterol, and Krawczyk (Reference KRAWCZYK2009) found lower cholesterol levels in the yolk of organic Greenleg Partridge chicken breed (12.89mg/100g yolk) compared to backyard (13.83mg/100g yolk) and conventional layers (13.93mg/100g yolk).
Zemkova et al. (Reference ZEMKOVA, SIMEONOVA, LICHOVNIKOVA and SOMERLIKOVA2007) studied the effects of laying hen housing in conventional cages, enriched cages, litter and outdoor systems on egg yolk and egg cholesterol concentration in ISA Brown hens. The highest cholesterol concentration of egg yolk (14.1 mg/100g yolk) and the whole egg (242.6 mg/egg) was in eggs from hens raised under the litter system, and the lowest in enriched cages (12.5 mg/100g yolk and 211.2 mg/egg). Cholesterol concentration in outdoor (13.4 mg/100g yolk and 228.5 mg/egg) and conventional system (13.3 mg/100g yolk and 231.2 mg/egg) ranged between the two systems mentioned above. Pištekova et al. (Reference PIŠTEKOVA, HOVORKA, VEČEREK, STRAKOVA and SUCHY2006) found a higher cholesterol content in egg yolk for ISA Brown floor-reared birds (1.17%) than in caged hens (1.12%)
As opposed to the above results, Cerolini et al. (Reference CEROLINI, ZANIBONI and LA COGNATA2005), Rizzi et al. (Reference RIZZI, SIMIOLI, MARTELLI, PAGANELLI and SARDI2006), Anderson (Reference ANDERSON2010) and Kucukyilmaz et al. (Reference KUCUKYILMAZ, BOZKURT, HERKEN, CINAR, CATH, BINTAS and COVEN2012) observed no effect of rearing system on egg cholesterol level.
Fatty acids
Fatty acid levels and ratio in all animal-derived foodstuffs have attracted the attention of researchers, due to the important effects of fatty acids on human health. Specific importance has been given to omega-3 and omega-6 fatty acids, and their ratio. An ideal ratio of omega-6 to omega-3 fatty acids is 10:1 or lower, as suggested by Simopoulos (Reference SIMOPOULOS1991; Reference SIMOPOULOS2000). Omega-3 polyunsaturated fatty acids have two major fields of interest. The first lies in their quantitative abundance and their role in the development and maintenance of the brain. The second is their role in the prevention of different pathologies, mainly the cardiovascular diseases, and latterly some psychiatric disorders, e.g. stress, depression and dementia. Thus, dietary omega-3 fatty acids are very important to ensure brain structure and function, more specifically during development and aging. Omega-3 FA enriched eggs alter the blood lipid profile of patients suffering from hypercholesterolemia, reducing plasma triglycerides and platelet aggregation (Bourre, Reference BOURRE2005). O'Brien and Andrews (Reference O'BRIEN and ANDREWS1993) found that omega-3 fatty acids in eggs have a beneficial effect on human health, and Samman et al. (Reference SAMMAN, KUNG, CARTER, FOSTER, AHMAD, PHUYAL and PETOCZ2009) reported that omega-3 eggs reduce risk factors for heart diseases.
However, with increasing polyunsaturated fatty acid (PUFA) content of poultry diets, there is a concomitant increase in the susceptibility to oxidative deterioration of eggs, leading to losses in quality characteristics and nutritional value, lower consumer acceptability and deleterious biological effects (Addis and Park, Reference ADDIS and PARK1989). Lipid oxidation is of great concern to the food industry because of the many undesirable flavours, colours, and potentially toxic reaction products that it causes in foods (Guérin-Dubiard et al., Reference GUÉRIN-DUBIARD, CASTELLANI and ANTON2007). The susceptibility of animal lipid to oxidation depends on a number of additional factors, including the concentration of pro-oxidants and antioxidants (Monahan et al., Reference MONAHAN, BUCKLEY, MORRISEY, LYNCH and GRAY1992).
Some reports indicate that n-3 PUFA are particularly susceptible to lipid oxidation, and even small differences in the concentration of these fatty acids may be critically important in the development of oxidation. Therefore, greater susceptibility to egg lipid oxidation may be expected in free range systems, as free range eggs are typically richer in PUFA (Lopez-Bote et al., Reference LOPEZ-BOTE, SANZ ARIAS, REY, CASTANO, ISABEL and THOS1998). However, the same author further stated that free range eggs commonly have a higher content of a-tocopherol, an important antioxidant, which makes the susceptibility to oxidation lower than would be expected solely on the basis of increased PUFA content. The increased content of PUFA and a-tocopherol in free range eggs appears to affect the oxidative stability of egg lipids through annulment of their effects, with the oxidative stability of such eggs typically being similar to that of conventional eggs. Miao et al. (Reference MIAO, GLATZ and RU2005) reported a similarity in oxidative stability between free range eggs, despite their increased n-3 PUF content, and conventional eggs. The content of a-tocopherol (vitamin E) in eggs from different rearing systems was dealt with in the section on vitamins.
Differences in fatty acid composition of eggs produced in various rearing systems result from different feeding regimens used (Naber, Reference NABER1979; Milinsk et al., Reference MILINSK, MURAKAMI, GOMES, MATSUSHITA and DE SOUZA2003; Szymczyk and Pisulewski, Reference SZYMCZYK and PISULEWSKI2003; Wang and Huo, Reference WANG and HUO2010). Cerolini et al. (Reference CEROLINI, ZANIBONI and LA COGNATA2005) compared four rearing systems: organic, outside access, floor housed or in battery cages. The fatty acid composition of total egg lipid in birds reared on the floor was significantly different compared to the fatty acid composition found in organic birds. The proportion of saturated fatty acids (SFA) was significantly lower, and polyunsaturated fatty acids (PUFA) was significantly higher in floor-kept birds compared to organic laying hens. The PUFA/SFA ratio was significantly higher in birds reared on the floor (0.92) compared to all other groups (organic 0.66; outside access 0.71; and battery cages 0.75). The proportion of n-3 PUFA was significantly lower in organic layers (1.51%) compared to all other groups (outside access 2.02%; floor reared 2.55%; and battery cages 2.16%).
Matt et al. (Reference MATT, VEROMANN and LUIK2009) evaluated the effect of rearing system (conventional vs. organic system) in Hy-Line Brown layers on the fatty acid profile of eggs. Eggs available from conventional production systems had a somewhat higher level of saturated fatty acids (2.5%) compared to organic eggs (2.3%), whereas the level of monounsaturated fatty acids was identical (3.2%). PUFA were higher in conventional laying hens, but the omega-6:omega-3 ratio was considerably more favourable in organic eggs (7:1) than in conventionally produced eggs (10:1). In their experiment with Comb White Leghorn layers under caged or free range systems, Lopez-Bote et al. (Reference LOPEZ-BOTE, SANZ ARIAS, REY, CASTANO, ISABEL and THOS1998) found that the amount of grass consumed can substantially affect egg quality. Since the complete feed used in the experiment was identical in both groups, the differences in fatty acid content can be wholly attributed to grass intake in free range birds. The total omega-3 fatty acid content of the yolk was almost three times lower in caged birds (1.16% vs. 3.02%), whereas the content of omega 6 fatty acids was higher (21.59% vs. 14.72%), giving the ratio of omega-6:omega-3 of 18.73:1 vs. 5.21:1. Karsten et al. (Reference KARSTEN, PATTERSON, STOUT and CREWS2010) determined omega-3 fatty acid concentration to be more than twofold greater under free range system where different plants were used as a ground cover (Alfalfa:Clover:Grass = 3.76%:3.59%:3.03%) than in a caged environment (1.28%). Therefore, although omega-6 fatty acid concentration did not significantly differ across the four systems, the ratio of omega-6:omega-3 fatty acids exhibited significant differences (Alfalfa:Clover:Grass:Caged = 4.44:4.76:5.70:12.05). Similar results were reported by Pavlovski et al. (Reference PAVLOVSKI, ŠKRBIĆ, LUKIĆ, LILIĆ, KRNJAJA, STANIŠIĆ and PETRIČEVIĆ2011), who compared Hy-Line Brown layers under free range and caged systems, and found no significant differences in the content of any fractions of fatty acids among rearing systems (SFA, MUFA, PUFA). However, omega-3 content was much higher in the eggs from free range hens (2.02%) than in caged birds (1.36%), and although omega-6 fatty acid content was similar (17.46% vs. 18.02%), the omega 6:omega 3 ratio was significantly different (8.64 vs. 13.25). The high effect of genotype on egg quality was highlighted by data on Naked Neck layers which were, in the same experiment, kept under free range system, resulting in considerably higher concentrations of omega-3 fatty acids (2.29%), and lower concentrations of omega-6 fatty acids (13.32%) in their eggs, resulting in an omega-6:omega-3 ratio as low as 5.81. These results agree with those of Simčić et al. (Reference SIMČIĆ, STIBILJ and HOLCMAN2011) who, in the indigenous Slovenian breed (Styrian), established 1.71% n-3 PUFA in eggs from hens reared in cages and 2.50 % n- 3 PUFA from hens kept free range. The content of n-6 PUFA in egg yolk from hens housed on free range was 14.93%. A higher content of omega-3 fatty acids in eggs from hens reared on grass was found by Van den Brand et al. (Reference VAN DEN BRAND, PARMENTIER and KEMP2004), Long and Alterman (Reference LONG and ALTERMAN2007), Robinson (Reference ROBINSON2007), Anderson (Reference ANDERSON2010).
Quite contrary results were published by Kucukyilmaz et al. (Reference KUCUKYILMAZ, BOZKURT, HERKEN, CINAR, CATH, BINTAS and COVEN2012). Namely, they reported higher levels of omega-3 fatty acids in eggs from caged Lohmann LSL (1.43%) and ATAK-S birds (1.72%) compared to organic laying hens (1.34% and 1.31%, respectively). The content of omega-6 fatty acids showed no significant difference between the systems, but the ratio of omega-6:omega-3 fatty acids was considerably higher in organic birds from both hybrids. The ratio of omega-6 to omega-3 fatty acids was 14.28 and 12.53 in organic Lohmann LSL and conventional eggs, respectively. In ATAK-S eggs, the ratio of omega-6:omega-3 fatty acids was drastically higher in the organic rearing system - 15.56 as opposed to only 11.95 for conventional birds. The explanation for these results provided by the authors was that, since the hens had rapidly depleted the pasture during the pullet rearing period, no vegetation was available during the egg laying phase.
Somewhat different results were published by Hidalgo et al. (Reference HIDALGO, ROSSI, CLERICI and RATTI2008), who observed no differences in fatty acid composition among conventional caged, free-range, floor, or organic labelled eggs, whereas Cherian et al. (Reference CHERIAN, HOLSONBAKE and GOEGER2002) observed similar levels of n-6 and n-3 in white eggs produced in conventional cages compared with eggs from certified organic, free-range brown hens. Holt et al. (Reference HOLT, DAVIES, DEWULF, GAST, HUWE, JONES, WALTMAN and WILLIIAN2011) explained this by the fact that, in both of these studies, there was no information on the feeds for the hens and thus no way to determine whether the cage eggs were from hens receiving feeds supplemented with these fatty acids. Likewise, Samman et al. (Reference SAMMAN, KUNG, CARTER, FOSTER, AHMAD, PHUYAL and PETOCZ2009) found no difference in the levels of omega-3 and omega-6 fatty acids in conventional and organic eggs purchased from supermarkets and health food stores. Differences were found only in the SFA fraction (higher in organic eggs). The comparison they made between omega-3 eggs and the other two groups suggested significant differences in the levels of omega-3 fatty acids and the fatty acid ratio, thus confirming the crucial effect of feed on the hen egg component analysed. Similar results were published by Poupoulis et al. (Reference POUPOULIS, SALEPI, SKAPETAS and TOUSKA2009) who determined the FA composition of egg yolks from farms using conventional, organic, free-range and omega-3 supplemented feeding. Results showed that the farming system significantly influenced the polyunsaturated fatty acid content, total omega-3 and omega-6 fatty acids as well as the ratios of PUFA:SFA and omega-6:omega-3 fatty acids. These researchers concluded that eggs produced with omega-3 supplemented feed had the best FA profile, followed by those from organically managed hens.
Hygienic conditions
With the increasing production of organic eggs for table consumption a greater number of laying hens are being housed in cage-free aviaries (litter area, slats, and nest boxes) and free-range (outdoor pasture access) conditions. The levels of bacterial contamination from alternative housing systems compared to conventional cage systems is an important factor influencing future food safety issues and regulations (Buhr et al., Reference BUHR, HANNAH, WILSON, COX, RICHARDSON, CASON and MUSGROVE2009). Eggshell contamination level at the time of egg collection has previously been shown to be directly related to the final contamination of egg products (Petrak et al., Reference PETRAK, PETRAK, JELIC, NEDJELI and HRASTE1999). Eggs from hens housed on litter were shown to have 15, or even 20 to 30 times more aerobic bacteria on the eggshells than eggs from hens housed in wire cages (Harry, Reference HARRY1963; Quarles et al., Reference QUARLES, GENTRY and BRESSLER1970). Eggs collected from conventionally caged laying hens compared with those from organic raised and housed laying hens (floor raised with outdoor access) and barn raised laying hens (indoor only) have been demonstrated to harbour fewer aerobic bacteria (De Reu et al., Reference DE REU, GRIJSPEERDT, HEYNDRICKX, ZOONS, DE BAERE, UYTTENDAELE, DEBEVERE and HERMAN2005b). The major differences found in experimental studies between cage and non-cage systems are less pronounced under commercial conditions.
The effect of housing systems on eggshell contamination with specific groups of bacteria is variable and limited. Recent research does not indicate large differences in egg contamination between those from cage- and non-cage systems (ignoring outside nest and floor eggs). The microflora of the eggshell is dominated by Gram-positive bacteria, whereas Gram-negative bacteria are best equipped to overcome the antimicrobial defences internally (De Reu et al., Reference DE REU, MESSENS, GRIJSPEERDT, HEYNDRICKX, RODENBURG, UYTTENDAELE and HERMAN2009).
De Reu et al. (Reference DE REU, GRIJSPEEDT, HEYNDRICKX, UYTTENDAELE and HERMAN2005a; Reference DE REU, GRIJSPEERDT, HEYNDRICKX, MESSENS, UYTTENDAELE, DEBEVERE and HERMAN2006) evaluated whether the differences in eggshell contamination found in experimental housing systems were also applicable to commercial conventional cage and non-cage housing systems. Two conventional cage systems, one organic aviary system and one floor housing system, were included. On average, higher (P<0.001) initial eggshell bacterial contamination was found for eggs from non-cage systems compared to conventional cage systems; 5.46 compared to 5.08 log CFU/eggshell respectively. However, initial contamination with total count of Gram-negative bacteria on the eggshells was significantly lower (P<0.001) in the non-cage systems; 3.31 compared to 3.85 log CFU/eggshell. These studies showed that the major differences in eggshell contamination found between conventional and non-cage systems in the experimental studies (>1 log), were lower in the commercial housing systems. The fact that even lower initial contamination with Gram-negative bacteria was observed in the commercial non-cage systems is remarkable.
Salmonella remains an important cause of human disease worldwide. In Europe, Salmonella enteritidis and S. typhimurium are the most commonly isolated serotypes in human cases of salmonellosis, and contaminated eggs still remain the most important source of infection with S. enteritidis for humans (De Jong and Ekdahl, Reference DE JONG and EKDAHL2006). Eggshells can become contaminated with salmonellae either as a result of infection in the oviduct or by faecal contamination. Eggshells can be contaminated with S. enteritidis as a result of intestinal carriage. Gast and Beard (Reference GAST and BEARD1992) reported a correlation between salmonella positive faeces and shell contamination after artificial infection of hens with S. enteritidis. The observed prevalence of salmonella and, particularly, that of S. enteritidis on the eggshell and in the egg content vary, depending on the fact whether investigations were based on randomly sampled table eggs or on eggs from naturally infected hens (De Reu et al., Reference DE REU, MESSENS, HEYNDRICKX, RODENBURG, UYTTENDAELE and HERMAN2008). Kinde et al. (Reference KINDE, READ, CHIN, BICKFORD, WALKER, ARDANS, BREITMEYER, WILLOUGHBY, LITTLE, KERR and GARDNER1996) stated that the increased exposure of layers to environmental contamination in non-cage systems would increase the risk of contamination with salmonella. Schaar et al. (Reference SCHAAR, KALETA and BAUMBACH1997) showed a significantly lower prevalence of S. enteritidis infections in caged laying hens compared to free range, while Mollenhorst et al. (Reference MOLLENHORST, VAN WOUDENBERGH, BOKKERS and DE BOER2005) found a significantly lower salmonella prevalence in laying hens housed in cage systems in comparison to deep litter systems. Unlike this, Methner et al. (Reference METHNER, DILLER, REICHE and BÖHLAND2006), Namata et al. (Reference NAMATA, MÉROC, AERTS, FAES, CORTINAS ABRAHANTES, IMBERECHTS and MINTIENS2008) and Van Hoorebeke et al. (Reference VAN HOOREBEKE, VAN IMMERSEEL, DE VYLDER, DUCATELLE, HAESEBROUCK, PASMANS, DE KRUIF and DEWULF2010) found lower prevalence of S. enteritidis infection in non-caged compared with caged rearing systems for laying hens. Commenting on the above results, Dewulf et al. (Reference DEWULF, VAN HOOREBEKE and VAN IMMERSEEL2009) concluded that it is highly unlikely that a move from conventional battery cage systems to alternative cage systems and non-cage housing systems for laying hens will result in an increase in salmonella infections and shedding; rather the opposite is expected. The true underlying causal mechanism that causes the prevalence of salmonella to be generally lower in alternative housing systems in comparison to cage systems has not been identified yet. It is likely to be a combination of factors influencing the infection pressure in the flock.
Conclusions
This paper provides a synthesis of the findings of many studies dealing with the effects of laying hen rearing systems on the egg chemical composition: proteins, fats, vitamins, cholesterol and fatty acids, as well as on the hygienic safety of eggs. Alternative laying hen rearing systems are an integral part of modern egg production. Husbandry systems for keeping laying hens have an impact on, inter alia, the chemical composition of eggs. Eggs from these laying hen rearing systems have been proven by a large body of literature data to have better nutritional properties.
The high variability in the chemical quality parameters of eggs is likely due to the effect of a variety of factors (genotype, age, nutrition, environment, pasture botanical composition, etc.). Each of the rearing systems analysed has both advantages and disadvantages. Future research should focus on investigations into both the nutritional quality (content and ratio of essential amino acids and proteins, content and ratio of saturated to unsaturated fatty acids, contents of vitamins and micro- and macronutrients) and the microbial contamination of eggs.
Acknowledgement
This study is part of the Project No. 31033 titled ‘Sustainable Conventional and Revitalized Traditional Production of Value-Added Poultry Meat and Eggs’ funded by the Ministry of Science and Technological Development of the Republic of Serbia.
