Quality of eggs from different laying hen production systems, from indigenous breeds and specialty eggs

Abstract

Consumers are concerned about the quality of commercially available eggs. Eggs used in this study were marketed in Portugal and originated from laying hens raised in cages, barns, free-range, organic eggs, and eggs enriched with n-3 polyunsaturated fatty acids (PUFA), and from native Portuguese breeds. The eggs were analyzed for chemical and physical properties. Results indicated that yolk color was lighter in organic eggs and darker in n-3 PUFA enriched eggs. Eggs from caged hens had lower Haugh units in contrast with organic eggs. Caged hens produced eggs with a higher protein content while organic eggs had the lowest level of protein in the albumen. As might be expected, eggs enriched in n-3 PUFA had the highest n-3 PUFA content. Choosing an egg by its production system or labeling specificities may not be a guarantee of superior product quality. The layer genotype, age, diet, and the quality of the range also may affect egg properties. Due to a different layer diet, enriched eggs seem to be of superior quality.

INTRODUCTION

Chicken eggs for human consumption are highly nutritious, palatable, inexpensive, and commonly available worldwide. In certain areas of the world, consumers are increasingly interested in chicken welfare and specialty eggs. In an effort to meet consumer demand, producers have begun marketing eggs that are laid by hens reared in alternative production systems, and with enhanced nutrient content. The most common laying hen rearing system is battery cages, which since 2012 in the European Union were modified to furnished cages in order to comply with the European Union Council Directive 1999/74/EC (EU, 1999a). Furnished cages must provide at least 750 cm² per hen, of which 600 cm² is 45 cm high, a nest, a littered area for scratching and pecking, 15 cm of perch and 12 cm of food trough per hen, and a claw shortening device. Alternative rearing methods include barn and free-range. Hens on a barn floor are raised free from cages but are kept entirely indoors, while in a free-range system hens are allowed access to the outside. Organic eggs are produced by hens reared in a free-range production system and fed organic feed that is free of genetically modified organisms and synthetic additives (EU, 1999b).

The increasing interest in poultry products from non-industrial production systems also triggers the attention of the consumer for more sustainable farming practices, allowing for indigenous breeds of poultry to be introduced and looked for in the market. Native breeds of chickens are adapted to the local environmental conditions and robust enough to withstand pathogens; however, little research attention has been given to these breeds.

The most common specialty eggs available in the market are the polyunsaturated fatty acid-enriched eggs. Decreased risk of cardiovascular disease and prevention and treatment of inflammatory diseases are some of the health benefits to humans that have been attributed to the consumption of n-3 polyunsaturated fatty acids (PUFA) (FAO, 2010). Eggs of this nature can be produced by laying hens that are fed different sources of n-3 PUFA, such as fish oils, linseed, or microalgae (Scheideler and Froning, 1996; Gonzalez-Esquerra and Leeson, 2000; Carrillo et al., 2008; Fraeye et al., 2012).

It has been reported that consumers are willing to pay extra for n-3 PUFA enriched eggs (Marshall et al., 1994). In addition, many consumers perceive organic eggs as a food product with a higher nutritional value and better taste and are therefore also willing to pay a premium price (Hansstein, 2011). However, as far as egg quality between production systems is concerned, scientific research is limited and has shown contradictory findings (Patterson et al., 2001; Van den Brand et al., 2004; Hidalgo et al., 2008; Anderson, 2011; Küçükyilmaz et al., 2012; Rakonjac et al., 2014).

When studying the differences among eggs for research purposes, breed, age, and/or diet (including the time spent and the quality of the outdoor range) of hens from which the eggs are produced are known. Therefore, it is widely accepted that those are the variables that play a larger role in the egg nutritional and physical properties (Van den Brand et al., 2004; Anderson, 2011; Küçükyilmaz et al., 2012;). Since information about breed, age, or feed formulation is not described on the labels of commercial eggs, consumers often make an uninformed purchase decision.

The objective of the current study was to compare a number of nutritional and physical characteristics, which are of interest to the consumer, among eggs that are available on the market shelves in Portugal. This included eggs from different housing systems, from indigenous breeds, and specialty eggs.

MATERIALS AND METHODS

Egg Sampling

One-hundred-and-forty-four commercially available grade A brown eggs were obtained from supermarkets. Eggs from 6 different origins were collected — undifferentiated eggs from laying hens raised in furnished cages (Cage), raised in barns (Barn), raised in a free-range (Free-R), organic eggs that do not discriminate the genotype of the hen (Org), eggs from hens in furnished cages but enriched with n-3 PUFA (En-3), and organic eggs from native breeds (Native). N-3 PUFA eggs originated from hens receiving extruded linseed in their diets. The native breeds that produced the eggs were Pedrês Portuguesa and Preta Lusitânica. All eggs were size M (between 53 and 63 g), with the exception of eggs from indigenous breeds that were size S (< 53 g), since this was the only egg category available. With the exception of protein and fatty acid analysis, eggs were examined the same d that they were purchased, and exactly 20 d before the expiration date so as to ensure consistent egg age. Analyses described below were performed in all eggs individually.

Analysis of Physical Characteristics, pH, and Protein Content

Whole eggs were individually weighed and candled to determine the percentage of eggs with pre-cracks. Eggshell color was scored using a scale from 1 through 6, with 1 being very light brown and 6 very dark brown. The eggshell color scale was created using 100 random brown eggs from different origins that were then ordered from lighter to darker. Eggshells from 6 equidistant points were used to establish the scale. Eggs were then opened and the eggshells were separated and dried in an oven for 24 h at 50ºC, after which they were weighed, to determine shell percentage. Blood and meat spots in the yolk and albumen were detected visually. Yolk color was scored using the Roche egg yolk fan (DSM, Heerlen, Netherlands). Thick albumen height was measured using a Baxlo micrometer (Baxlo Precision, Barcelona, Spain), followed by the calculation of Haugh units (Haugh, 1937) using the formula 100^*log(h–1.7^*w^0.37 + 7.57), where h is the height of the thick albumen and w is the egg weight.

The thick and the thin albumen were separated from the yolk with a pipette to guarantee that the vitelline membrane of the yolk would be intact and without any albumen residue. One mL of each intact albumen was used to measure the viscosity of the thick and thin albumen separately using a viscometer with a spindle at 6 rpm (Model LVDVCP-II, Brookfield Engineering Laboratories, Middleboro, MA). Intact yolk was weighed for determination of yolk percentage and albumen weight was calculated by difference. Albumen pH was determined using a potentiometer 744 pH Meter (Metrohm, Herisau, Switzerland). Albumen was analyzed for nitrogen content using the Kjeldahl method and the conversion factor from nitrogen to protein was 6.25.

Determination of Fatty Acid Composition

Prior to fatty acid preparation, yolk samples were freeze-dried (ScanVac CoolSafe, Labogene, Lynge, Denmark) and homogenized. Fatty acid methyl esters (FAME) were prepared by a direct transesterification procedure with the addition of 19:0 (one mg/mL) as internal standard. Briefly, one mL of toluene was added to 100 mg of yolk sample, then 2 mL of sodium methoxide in methanol (0.5 N) were added and after reaction for about 10 min at 50ºC, another 3 mL of 10% HCl in methanol were added to the reaction vessel and left to react for more 10 min at 80ºC. After cooling, samples were neutralized with 6% aqueous potassium carbonate and FAME were extracted with hexane. The solvent was removed under a flow of nitrogen at 37°C and the final residue was dissolved in 1.5 mL of hexane, and stored at −20°C until gas chromatography (GC) analysis. FAME were quantified by fast-GC using a Shimadzu GC-2010 Plus chromatograph (Shimadzu, Kyoto, Japan) equipped with a Suprawax280 capillary column (10 m, 0.10 mm i.d., 0.10 μm film thickness, Teknokroma, Barcelona, Spain) and a flame ionization detector (FID). Helium was used as carrier gas at a constant pressure of 296.7 kPa, and the injector and detector were maintained at 280°C. Column oven programmed temperatures were as follows: The initial oven temperature of 120°C was increased to 175°C at 35°C/min and held for 0.5 min, then increased to 260°C at 70°C/min and was maintained for more 15 min. Identification of FAME was achieved by comparison of the FAME retention times with those of authentic standards (FAME mix 37 components from Supelco Inc., Bellefont, PA). Additional identification of the FAME was achieved by electron impact mass spectrometry using a Shimadzu GC-MS QP2010 Plus (Shimadzu, Kyoto, Japan). The mass spectrometer conditions were as follows: ion source temperature, 200°C; interface temperature, 220°C; ionization energy, 70 eV; scan, 50 to 500 atomic mass units.

The total fatty acid content in yolk samples was calculated using an internal standard and assuming direct proportionality between GC-FID peak area and FAME weight. The results for each FA were expressed as a percentage of the sum of detected FA (g/100 g of total FA).

We calculated the fatty acid content in yolks (mg/g of yolk), assuming a yolk water content of 52.3 g/100 g as indicated in the USDA food composition database.

Statistical Analysis

Data were analyzed using one-way analyses of variance. Differences between means were tested using the Duncan's test by the GLM procedure of SAS (SAS Institute, 2012). Frequency of eggs with blood or meat spots and with cracks was analyzed by the GLIMMIX procedure of SAS (SAS Institute, 2012) using the binary distribution and the logit link function. All statements of significance were based on testing at the P < 0.05 level.

RESULTS

Physical Characteristics, pH, and Protein Content

Even though the eggs that were collected were all size M, it was found that the weights of Cage and En-3 eggs were heavier (P < 0.05) than the Org eggs. Native breeds were not selected for specific egg production traits and the only egg size available for purchase is small. The percentage of yolk was higher (P < 0.05) in En-3 and Cage eggs in comparison to Org and Native eggs (Table 1). In contrast, albumen percentage was higher (P < 0.05) in Org and Native eggs than in the remaining groups. No differences were found in the percentage of shell among eggs from different origins (Table 1). Shell color was found to be darker in En-3 PUFA and Cage eggs, and lighter in Native eggs (P < 0.05).

Table 1.

Mean comparison of quality characteristics of eggs with different labels.

	Egg label1						Significance
	Cage	Barn	Free-R	Org	En-3	Native	SEM	P(F)
Egg components
Whole egg (g)	60.30a	59.08a,b	59.16a,b	58.23b	60.57a	46.40*	0.478	0.026
Yolk (%)	27.05a	26.09a,b	25.72a,b	24.16c	26.60a	24.75b,c	0.230	0.001
Albumen (%)	62.49b	63.39b	64.10a,b	65.54a	63.19b	65.24a	0.242	<0.001
Shell (%)	10.47	10.52	10.17	10.30	10.21	10.01	0.058	0.097
Shell color	3.83ª	3.17b	3.04b	2.88b	3.88ª	1.96c	0.094	<0.001
Albumen pH	9.28a	9.28a	9.28a	9.10b	9.24a	9.29a	0.009	<0.001
Haugh units	48.39e	58.12c	55.40c,d	65.26b	50.31d,e	75.59a	1.116	<0.001
Albumen protein (%)	11.63a,b	11.20b–d	11.09c,d	11.02d	11.71a	11.51a–c	0.067	0.005
Yolk color	12.08b	12.29b	12.54b	6.04c	13.79a	1.38d	0.382	<0.001
Albumen viscosity (mPa.s)
Thick albumen	38.70	40.41	40.53	43.03	42.18	45.23	0.652	0.062
Thin albumen	25.21b	25.73b	25.18b	25.84b	30.72a	27.78a,b	0.555	0.024

¹Eggs from laying hens raised in furnished cages (Cage), raised in barns (Barn), raised in a free-range (Free-R), organic eggs (Org), eggs enriched with n-3 PUFA (En-3) and eggs from native breeds (Native).

^a–dMeans with no common superscripts are different (P < 0.05).

^*Eggs not used for mean comparison as they were of a different weight category from the remaining eggs.

Albumen pH was lower (P < 0.05) in Org eggs in comparison to the remaining groups of eggs. Haugh unit (HU) score was higher in eggs from native breeds, followed by Org eggs. Caged hens, with and without n-3 PUFA supplementation, produced eggs with the lowest (P < 0.05) HU score, followed by Barn and Free-R eggs (Table 1). In comparison to eggs laid by hens reared in cages (Cage and En-3), Free-R and Org eggs had significantly lower (P < 0.05) protein content in the albumen (Table 1). Yolk color was significantly lighter in organic eggs (Org and Native) in comparison to the remaining eggs. N-3 PUFA enriched eggs had the darkest yolk color (Table 1). Viscosity of the thick albumen was not different among groups. However, the viscosity of the thin albumen was higher (P < 0.05) in the En-3 eggs in comparison to the remaining groups (Table 1).

No differences were found in the frequency of blood spots and meat spots in the yolk and albumen of eggs from the different groups. The results show that En-3 eggs presented higher (P < 0.05) frequency of shell cracks than the other groups with the exception of Cage eggs (Table 2).

Table 2.

Frequency (%) of blood spots, meat spots, and shell cracks in eggs with different labels.¹

	Cage	Barn	Free-R	Org	En-3	Native	P(F)
Blood spots	20.8 ± 8.29	41.7 ± 10.7	37.5 ± 9.88	41.7 ± 10.1	25.0 ± 8.84	29.2 ± 8.28	0.519
Meat spots	20.8 ± 8.29	29.2 ± 9.28	8.3 ± 5.64	8.3 ± 5.64	8.3 ± 5.64	4.1 ± 4.08	0.141
Shell cracks	25.0a,b ± 8.84	8.3b ± 5.64	4.2b ± 4.08	8.3b ± 5.64	33.3a ± 9.62	4.2b ± 4.08	0.036

¹Eggs from laying hens raised in furnished cages (Cage), raised in barns (Barn), raised in a free-range (Free-R), organic eggs (Org), eggs enriched with n-3 PUFA (En-3) and eggs from native breeds (Native).

^a,bMeans with no common superscripts are different (P < 0.05).

Fatty Acid Composition

Fatty acid profile of the eggs, expressed as g/100 g of total fatty acids, is shown in Table 3. Oleic acid (18:1 cis-9), palmitic acid (16:0), and linoleic acid (18:2 n-6) are the most abundant fatty acids in all egg types, comprising about 80% of total fatty acids. As expected, the En-3 eggs presented a fatty acid profile quite distinct from the other egg types, with highest proportions of linolenic acid (18:3 n-3), n-3 docosapentaenic acid 22:5 n-3 (DPA), and docosahexaenoic acid 22:6 n-3 (DHA), and the lowest proportions of 16:0, 18:2 n-6, 20:0, 20:2 n-6, 20:4 n-6, 22:4 n-6, and n-6 docosapentaenoic (n-6 DPA, 22:5 n-6). The Eicosapentaenoic acid 20:5 n3 (EPA) was not detected in all egg types. In spite of the significant differences observed for all fatty acids, it can be noticed that proportions of saturated fatty acids (SFA) vary within a smaller range than monounsaturated fatty acids (MUFA) and PUFA. In fact, SFA ranged from 30% in En-3 eggs to 35% of total fatty acid in Native eggs. The MUFA, comprised mostly by 18:1 cis-9, ranged from 37% in Barn eggs to 45% of total fatty acids in Cage eggs. The PUFA proportions ranged from 20% in Cage and Native eggs to 30% of total fatty acids in Barn eggs.

Table 3.

Mean comparison of fatty acid composition (g/100 g of fatty acids) of eggs with different labels.

	Egg label1						Significance
	Cage	Barn	Free-R	Org	En-3	Native	SEM	P(F)
14:0	0.30b	0.24c	0.22c	0.29b	0.23c	0.37a	0.006	<0.001
14:1 cis-9	0.06b	0.02d	0.04c	0.04c	0.04b,c	0.08a	0.001	<0.001
15:0	0.07b	0.07b	0.07b	0.08a	0.06c	0.07a,b	0.001	<0.001
16:0	24.61a	22.49c	22.60b,c	23.36b	21.26d	25.03a	0.156	<0.001
16:1 cis-9	3.50a	1.57c	1.88c	2.50b	2.66b	3.46a	0.083	<0.001
17:0	0.16b	0.25a	0.24a	0.24a	0.17b	0.24a	0.005	<0.001
17:1 cis-9	0.16b,c	0.14d	0.16c,d	0.17a,b	0.19a	0.18a	0.002	<0.001
18:0	7.44c	7.91b	7.81b,c	8.05b	8.19b	8.74a	0.066	<0.001
18:1 cis-9	41.44a	34.75d	37.02c	34.88d	40.63a	39.10b	0.275	<0.001
18:2 n-6	15.67c	25.72a	23.66b	22.43b	16.22c	14.71c	0.438	<0.001
18:3 n-3	0.47c	0.43c	0.37c	0.91b	4.44a	0.45c	0.137	<0.001
20:0	0.24a	0.23a	0.23a	0.19b	0.17c	0.24a	0.003	<0.001
20:2 n-6	0.14c	0.30a	0.25b	0.23b	0.12d	0.17c	0.007	<0.001
20:3 n-6	0.15b,c	0.15b,c	0.15b	0.21a	0.13c	0.12a	0.003	<0.001
20:4 n-6	1.80d	2.16b	1.95c	2.21b	1.04e	2.50a	0.043	<0.001
22:4 n-6	0.15c	0.24a	0.20b	0.16c	0.06d	0.25a	0.006	<0.001
22:5 n-6	0.53b,c	0.62a	0.51c	0.25d	0.01e	0.59a,b	0.021	<0.001
22:5 n-3	0.07d	0.09c,d	0.07d	0.11c	0.24a	0.16b	0.007	<0.001
22:6 n-3	0.60d	0.45e	0.47e	0.98b	1.67a	0.82c	0.037	<0.001
Sums
SFA	32.8b	31.1c	31.2c	32.2b	30.1d	34.7a	0.17	<0.001
MUFA	45.2a	36.5d	39.1c	37.6d	43.5b	42.8b	0.33	<0.001
Total PUFA	19.6d	30.2a	27.6b	27.5b	24.2c	19.9d	0.45	<0.001
n-6 PUFA	18.3c	28. 9a	26.5b	25.3b	17.5c	18.3c	0.46	<0.001
n-3 PUFA	1.13d	0.97d	0.91d	2.00b	6.66a	1.43c	0.174	<0.001
Total fatty acid2	523b,c	520b,c	524b,c	500c	566a	530b	6.4	<0.001

¹Eggs from laying hens raised in furnished cages (Cage), raised in barns (Barn), raised in a free-range (Free-R), organic eggs (Org), eggs enriched with n-3 PUFA (En-3) and eggs from native breeds (Native).

²mg/g yolk dry matter.

^a–dMeans with no common superscripts are different (P < 0.05).

Total fatty acid content and nutritionally relevant sums of fatty acids, expressed in mg/g of yolk, are presented in Table 4. The n-3 PUFA enriched eggs presented the highest fatty acid content (4,344 mg/g yolk). Eggs originating from caged hens (Cage and En-3) presented the highest level of SFA and MUFA (P < 0.05). As expected, En-3 eggs presented the highest content of n-3 PUFA (296.1 mg/g yolk).

Table 4.

Mean comparison of fatty acids content in yolks (mg/yolk) of eggs with different labels.¹

	Egg label1						Significance
	Cage	Barn	Free-R	Org	En-3	Native	SEM	P(F)
SFA	1,367a	1,216c	1,211b,c	1,105c,d	1,335a,b	1,046d	32.7	<0.001
MUFA	1,879a	1,427b,c	1,519b	1,292c	1,933a	1,286c	43.2	<0.001
n-6 PUFA	771b	1,137a	1,043a	876b	780b	542d	30.3	<0.001
18:2 n-6	657b	1,003a	924a	770b	720b	434c	29.2	<0.001
n-6 LC PUFA2	115b,c	134a	119b	106c	60d	109c	2.48	<0.001
n-3 PUFA	47.7c	37.8c	35.3c	68.6b	296.1a	42.4c	4.69	<0.001
18:3 n-3	19.7b,c	16.9b,c	14.5b,c	31.4b	211.0a	13.6c	4.28	<0.001
22:5 n-3	3.0b,c	3.3b,c	2.8c	3.7b,c	10.7a	4.6b	0.41	<0.001
22:6 n-3	25.0c	17.6d	18.1d	33.5b	74.4a	24.2c	1.29	<0.001
Total PUFA	819c	1,175a	1,078a	944b,c	1,076a,b	585d	32.6	<0.001
Total fatty acids	4,065a,b	3,818b	3,808b	3,342c	4,344a	2,917d	89.6	<0.001

¹Eggs from laying hens raised in furnished cages (Cage), raised in barns (Barn), raised in a free-range (Free-R), organic eggs (Org), eggs enriched with n-3 PUFA (En-3) and eggs from native breeds (Native).

²Sum 20:2 n-6, 20:3 n-6, 20:4 n-6, 22:4 n-6, 22:6 n-6 and 22:5 n-6.

^a–dMeans with no common superscripts are different (P < 0.05).

DISCUSSION

Physical Characteristics, pH, and Protein Content

The proportion of egg components is affected by hen strain and age (Akbar et al., 1983). As the hen ages, the percent yolk increases and albumen decreases (Fletcher et al., 1981; Van den Brand et al., 2004). Egg component yields may have little importance to the consumer but they are significant to the egg processing industry, as yolk has a higher market value (Fletcher et al., 1981). In the present study, eggs from hens raised in an organic production system (native and organic) presented a higher albumen and lower yolk percentage relative to the whole egg. Other than the type of husbandry system, this difference may have been attributable to the hen's age and breed.

Shell failures represent an important economic concern for the egg industry, and, thus, egg cracks should be minimized. When analyzing eggs from different weight categories, it has been reported that shell percentage is lowest in larger eggs (Casiraghi et al., 2005; Hidalgo et al., 2008). In the present study, however, and considering that only one egg weight category was analyzed, shell percentage remained not different among production systems while differences were found between egg weights, with caged hens (Cage and En-3) producing heavier eggs. Nevertheless, shell pre-cracks were more prevalent in eggs laid by caged hens. In other studies, Patterson et al. (2001) indicated greater egg breaking and leakage in specialty eggs than in regular eggs. The appearance of shell cracks is a result of the combination of shell content, thickness, shell strength and integrity, and the extent of the trauma received by the egg during handling (Hunton, 2005). Genetics also plays a significant part in eggshell quality, and, therefore, the breed is likely an important factor affecting shell characteristics.

Shell color is not an indication of the nutritive value or the quality of the egg. However, many consumers who prefer brown eggs also pay attention to the intensity and consistency of the colors of the shells in the egg cartons (Cavero et al., 2012). Since the heritability of eggshell color is relatively high (Zhang et al., 2005), commercial brown-egg lines have been selected for dark brown shells for many years. Differences found in eggshell color in the current study may have been due to differences in breed or age. The considerable lighter color of eggshells laid by the native breeds may have been due to their differentiated genetic background. The reason caged hens laid darker eggshells is unlikely due to their production system, but rather to their age or physiological state. Older hens tend to lay larger eggs with lighter shell color because the quantity of protoporphyrin pigments deposited on the shell surface does not increase in proportion to egg size (Solomon, 1997). In addition, pigment is added to the shell late in the shell formation process, hence, poor pigmentation may occur if the egg is laid prematurely (Nys et al., 1991).

It has been shown that albumen pH is determined almost entirely by storage time and that is a reliable predictor of egg quality and freshness (Silversides & Scott, 2001). As the egg ages, it loses water and carbon dioxide, which leads to an increase in albumen pH. Although eggs analyzed in the present study had the same age and were obtained from supermarkets that store them at room temperature (a common practice in supermarkets in southern Europe), it was found that organic eggs had a lower pH. Eggs produced from native breeds, although also being organic, did not have a different pH from those of the remaining production systems. This may indicate that factors other than housing system, storage time, and condition may influence the pH of the albumen. It has been reported that albumen pH may decrease with layer age (Lapão et al., 1999; Silversides and Scott, 2001).

Other than the pH, the egg industry also measures HU as a way of assessing egg quality by adjusting the height of the albumen with the weight of the egg in a logarithmic scale — a higher HU indicates a better internal egg quality (Haugh, 1937). There are many factors that affect HU values such as age and strain or breed of the hen as well as time of storage and storage conditions, dietary ingredients, and possible disease (Williams, 1992; Roberts, 2004). In this study, it was found that hens from both organic production systems and native breeds (Org and Native) produced eggs with higher HU values; however, authors who have studied HU in different rearing systems present contradictory results. While some authors found higher a HU score in caged hens (Patterson et al., 2001; Hidalgo et al., 2008), others found a higher score in organic or free-range systems (Castellini et al., 2006; Dukić-Stojčić et al., 2009), or no difference among production systems (Küçükyılmaz et al., 2012). Even though HU score is an important measure of egg quality, it may be difficult to assess HU by the production system alone. All other commercial factors may play an important role in internal albumen quality.

A higher protein content was found in the albumen of eggs from caged hens (Cage and En-3), in contrast to Free-R and Org eggs. It is well established that the protein content of the egg is highly influenced by the diet of the hen (Csonka and Jones, 1952). Furthermore, Shafer et al. (1996) reported that the intake of additional dietary methionine results in the production of eggs with more protein. Since methionine supplements are banned from organic diets for laying hens in the EU, it is entirely possible that caged hens have continuous access to a more balanced diet that meet their requirements and therefore produce a more nutritious egg.

A darker yolk color is highly desirable by European consumers and is largely affected by feed, mainly by the presence of xanthophyll (Karunajeewa, 1978). In the present study, En-3 eggs contained a darker yolk color. Yolk color was markedly lighter in eggs laid by hens raised in organic systems (Org and Native). This finding is in accordance with other authors who reported darker yolk color in caged hens in comparison to alternative production systems (Hidalgo et al., 2008; Küçükyılmaz et al., 2012). In the EU, the organic feeds that are given to poultry cannot contain sources of synthetic xanthophyll, which most likely accounts for the low yolk pigmentation in organic eggs. On the other hand, several authors have reported darker yolk colors in eggs produced by hens in free-range systems because of the access to feedstuffs rich in carotenoid pigments such as grass and herbs (Van den Brand et al., 2004; Mugnai et al., 2009). However, it should be taken into account that the quality of the range is not always consistent and these grass and herbs may not be available throughout the year. Furthermore, even though the outdoors is accessible in free-ranging systems, only a small proportion of the flock is outside at any given time (Keeling et al., 1988; Zeltner and Hirt, 2003).

Viscosity of the thick and the thin albumen is a characteristic that is often overlooked. There is little or no information concerning the factors that affect albumen viscosity. However, this can be an important property as it is related to the whipping, emulsifying, and gelling properties of the albumen (Kemps et al., 2010). For the egg product industry, further knowledge related to the rheological properties of eggs is needed to better serve the growing consumer demand for processed egg products (Kumbár et al., 2015). As expected, in this study, the viscosity of the thick albumen was consistently higher than the viscosity of the thin albumen. No differences were found in the thick albumen viscosity between types of eggs. However, En-3 eggs had a higher thin albumen viscosity that may be due to a lower degree of destabilization of albumen protein complexes by these hens, due to possibly their younger age and/or diet.

Fatty Acid Composition

The fatty acid composition of the eggs was highly variable probably reflecting differences in the diets of hens. Nevertheless, it is clear that collectively SFA were less variable than MUFA and PUFA as noted previously (Fraeye et al., 2012).

The egg yolk is designed to supply the required PUFA supply for the development of the embryo and thus contain between 15 to 26% of total fatty acids of C18 PUFA and 3.3 to 4.6% as C20 and C22 PUFA. Eggs can easily be enriched with n-3 PUFA by modification of the diets fed to laying hens (Fraeye et al., 2012). In fact, the egg from hens fed extruded linseed presented an increased abundance of 18:3 n-3 and a more moderate increase in DHA (22:6 n-3) accompanied by a relevant reduction of 18:2 n-6, 20:4 n-6 and other n-6 PUFA like 22:5 n-6. No EPA (20:5 n-3) were detectable in any type of eggs, as the conversion of EPA to DHA seems to be particularly efficient in the liver of hens (Fraeye et al., 2012).

Long chain n-3 PUFA, as EPA and DHA, are known to reduce the risk of certain chronic diseases and the lower acceptable intake for adults is 250 mg/day (FAO, 2010). Chicken eggs contain only negligible amounts of EPA but contain DPA n-3, which can be easily retro-converted back to EPA (Kaur et al., 2011). Thus, each yolk of En-3 eggs provides about 85 mg of long chain n-3 PUFA (one-third of the daily recommended intake). The yolks of the other types of eggs have lower but still relevant content of long chain n-3 PUFA (21 to 37 mg) and, thus, each yolk supplies about 8 to 15% of daily recommended intake for these PUFA. The consumption of eggs, and particularly of En-3 eggs, does not seem to have negative effects on serum lipids in the majority of the population and is particularly important in regions of the world where fish (a food product naturally high in long chain n-3 PUFA) consumption is low (Lewis et al., 2000).

CONCLUSION

The present study demonstrates that there is little relation among the different egg labels and the quality characteristics of the egg except for the n-3 PUFA content. Other factors, such as breed, diet, and age are likely to play a more important role in egg properties. In addition, as far as free-range production systems are concerned (including organic), the quality of the pasture, the season, and the amount of time the hen spends outdoors are very important factors that affect egg quality but are difficult to control. Furthermore, this information is not accessible to the consumer and therefore the buyer is making a less-informed purchasing decision as far as egg quality is concerned. We established that it is difficult to predict egg quality by the production system alone. However, we also demonstrated that specialty eggs labeled “omega-3 enriched” are indeed of greater quality in relation to their fatty acid profile in the yolk as well as yolk color and albumen protein content.