Livestock Research for Rural Development 26 (11) 2014 | Guide for preparation of papers | LRRD Newsletter | Citation of this paper |
Concerns about the quality of eggs produced by hens and consumer acceptable production methods have led to a search for alternative housing systems. This study examined the effects of rearing systems {deep litter system (DL), with or without access to legumes (LP) or grass (GP) pasture} on egg quality of ISA Brown layers. A total of 240 ISA Brown birds were used for the study. Eighty were assigned to each treatment, replicated four times at 20 birds each. Daily egg production records were kept starting from the day of first egg to 42 weeks in lay. Egg quality characteristics were determined at 24, 38 and 60 weeks of age. Egg quality which included egg weight, egg length, egg width, yolk weight, yolk height, albumen weight, albumen height, shell thickness, yolk colour, yolk index, egg shape index, albumen index, specific gravity, haugh unit and cholesterol content were determined.
Egg shell thickness (mm) was higher (P<0.05) in GP (0.58) and LP (0.47) than in DL (0.38) at 60 weeks of age. Also, the egg yolk colour was deeper (P<0.05) in GP (3.00+0.00) and LP (2.25) than in DL (1.00) at 60 weeks of age. Cholesterol level was lower (P<0.05) in the eggs obtained from GP (518+3.38) and LP (511+2.01) than DL (528+4.27) at 60 weeks of age. The findings in this study clearly show that rearing layers birds with access to pasture consumption enhanced egg quality parameters and that the type of pasture may influence the quantitative effect of the quality measure and timing of access during lay. Rearing chicken on pasture resulted in eggs with greater shell thickness.
Key Words: alternative housing, egg characterisitcs, forage, hen
As a result of the dramatic improvement in poultry production over the last few decades, production capacity has increased with the use of technologies targeted at improved breeding and genetics, enhanced nutrition and development in housing systems. High levels of mechanization are used in production methods including housing system, egg collection, ventilation, feeding, lighting and waste handling (Blokhuis 2004). The use of battery cages for laying hens has been banned since January, 2012 in Europe and some other parts of the world as a result of consumers’ concerns for the welfare of the birds and the quality of the eggs produced by them. This implies that alternative housing systems including pastured poultry or outdoor systems must be developed. Consequently, there has been a renewed interest in free-range poultry farming in developed countries (Karsten et al 2010; Sun et al 2012).
Pastured poultry relies on raising chickens partly on pasture. The model has been developed over the last twenty years and allows the birds to receive a significant amount of pasture forage as feed. The practice of pasture-raised poultry provides chickens with fresh pasture and small quantities of insects, and worms (Glatz et al 2005), which in turn can lead to enhanced quality of eggs. It also allows the chicken to exercise and to express their natural repatoir of behaviours. In the last two decades, the quality of chicken egg has been an area of primary consumer concern, due to the connection between specific dietary lipids and the development of coronary heart disease and some forms of cancer (Simopoulos and Salem 1992). Transportation of eggs without damage to egg shell has been a major concern to marketers. Producing eggs with thicker egg shell will therefore be an added advantage to marketers. There is a dearth of information on the effect of pasture on egg shell thickness. Nworgu et al (2012) however reported that supplementation with basil (Ocimum gratissimum) leaf did not have effect on the thickness of egg shell.
The resultant effects of alternative systems for egg quality are currently unclear. Torges et al (1976) have described the effects of different housing systems, but there has been little research on egg quality of current breed in outdoor systems (Leyendecker et al 2001). It is hypothesized that breeds may differ in their reaction to outdoor systems or to the types of pastures offered. Most of the research on the effects of housing systems on egg production has been carried under temperate conditions but limited in the humid tropical region. The aim of the present study was to investigate the effects of access to grass or legume pastures by layers housed under deep litter systems in the humid tropical South Western Nigeria, where exotic layer strain dominate the table egg production market, on egg quality.
This study was conducted at the Teaching and Research Farms Directorate (TREFAD), Federal University of Agriculture, Abeokuta, Ogun State, Nigeria.
Prior to the establishment of the paddock, the land was ploughed and harrowed. The grass species Cynodon dactylon was established vegetatively (sprigs). The sprigs were planted at 7m³/ha into a well prepared seedbed. The legume pasture was established using Stylosanthes hamata seeds that were sown at the rate of 3kg of seed/ha. Irrigation was practiced during the dry season. The chemical compositions of the pastures are shown in Table 1.
Table 1 : Proximate composition of Cynodon dactylon and Stylosanthes hamata (On DM basis except for DM which is on "fresh" basis) |
||
Cynodon dactylon |
Stylosanthes hamata |
|
Dry matter (%) |
23.2 |
18.8 |
Crude protein (%) |
2.10 |
4.16 |
Fibre content (%) |
1.02 |
1.16 |
Carbohydrate (%) |
14.36 |
10.01 |
Ash content (%) |
1.18 |
1.07 |
Sodium (mg/g) |
2.12 |
2.67 |
Potassium (mg/g) |
6.78 |
4.66 |
Phosphorus (mg/g) |
1.27 |
2.12 |
Magnesium (mg/g) |
0.73 |
0.61 |
Calcium (mg/g) |
0.77 |
0.77 |
Iron (mg/g) |
1.24 |
1.89 |
Zinc (mg/g) |
0.01 |
0.02 |
Prior to the arrival of the chicks, the brooding pen was washed, disinfected and covered with polythene nylon to prevent heat loss. The feeders and drinkers were washed and disinfected. The brooding pen floor was littered to an even depth of 8 cm with wood shavings. Feeders, drinkers and heat source were provided.
A total number of 240 day-old chick pullets of a commercial strain (Isa Brown) were purchased from a reputable commercial farm. Chicks were brooded at a temperature of 35 °C at one day of age. The temperature was reduced gradually until the birds developed enough feathers. The temperature was reduced gradually by reducing heat supply and opening up the side covers.
At 12 weeks old, the birds were housed under three experimental groups viz. deep litter (DL), deep litter with access to a grass-based pasture (GP) and deep litter with access to a legume-based pasture (LP). The size of the pasture used in each of the replicate was 80m2. Birds were assigned to the deep litter houses at 20 birds/pen with 4 replicate pens per treatment. Nesting boxes, perches, feeding and water troughs were provided in the houses. The compositions of the poultry feed used during the experimental period are shown in Table 2.
Wood shaving at a depth of 8 – 10cm was used as bedding. Routine and occasional management practices in poultry production were carried out. Feeders and drinkers were cleaned, litter was changed as at when due, and vaccination and medication schedule were strictly adhered to.
Table 2: Percentage Composition of experimental diet (DM basis) |
|||
Ingredients |
Chick mash |
Grower Diet |
Layer Diet |
Maize |
46.50 |
40.00 |
48.00 |
Corn bran |
....... |
16.00 |
....... |
Soybeans |
14.40 |
10.00 |
11.00 |
Groundnut cake |
6.80 |
6.00 |
8.75 |
Palm kernel cake |
....... |
10.00 |
5.00 |
Fish meal |
1.70 |
2.00 |
1.50 |
Wheat offal |
25.20 |
10.19 |
14.00 |
Bone meal |
2.40 |
3.00 |
2.50 |
Oyster shell |
2.00 |
2.00 |
...... |
Limestone |
...... |
....... |
8.50 |
Salt |
0.25 |
0.25 |
0.25 |
*Premix |
0.25 |
0.25 |
0.25 |
Lysine |
0.25 |
0.20 |
0.10 |
Methionine |
0.25 |
0.11 |
0.15 |
Total |
100 |
100 |
100 |
Calculated analysis |
|||
Crude protein (%) |
19.04 |
16.22 |
17.13 |
Crude fibre (%) |
4.15 |
4.51 |
4.30 |
Ether extract (%) |
3.75 |
3.99 |
4.30 |
Calcium (%) |
1.47 |
2.00 |
4.11 |
Phosphorus (%) |
0.46 |
0.69 |
0.92 |
Methionine (%) |
0.55 |
0.47 |
0.44 |
Lysine (%) |
1.06 |
0.82 |
0.88 |
Metabolisable energy (Kcal/kg) |
2,650.22 |
2851.00 |
2,489.05 |
*Supplied per kg diet: Biotin = 40mg; Zn = 58mg; Fe = 5800mg; Vit A = 1,000,000 i.u ; Folic acid = 500mg; Se = 120mg; I = 60mg; Nictotinic acid = 2800mg; Cu = 700mg; Mn = 4800mg; Vit K = 1,500mg; Riboflavin = 500mg; Co = 300mg. |
Five eggs were selected at random from each replicate at 24, 38 and 60 weeks of age of the laying birds. They were weighed and the following quality parameters were determined: egg weight, albumen Index, eggshell thickness, egg specific gravity, Haugh Units, egg yolk colour, egg weight, yolk index and egg Shape Index.
Egg weight (g): The Egg Weight (EW) was measured with an electronic balance to the nearest 0.01 g.
Yolk Index (YI): This was calculated using the following formula as described by Doyon et al (1986):
YI = YH x 100
YW
Where YI = Yolk index
YH = Yolk height
YW = Yolk width
Shape Index: The shape index was calculated using the following formula (Anderson et al 2004):
SI = W X 100
L
Where : W = Width of egg
L = Length of egg
Albumen Index (AI): This was calculated with the following formula (Doyon et al 1986):
AI = ( AH) X 100
(AL + AW)/2
Where AI = Albumen index AH = Albumen Height AL = Albumen Length AW = Albumen width The albumen height was measured using P6085 spherometer (tripod micrometer) with 0.01mm accuracy in a flat dish |
Egg shell thickness; Thickness was measured after removing the internal membranes of the eggshell. A precision micrometer was used to the nearest 0.01mm (Mitutoyo Dial Thickness Gage). Measurements were taken at the three regions of the shell and the means were calculated.
The assessment of the eggs’ specific gravity was based on Archimedes’ principle. The eggs were weighed in air on a Mettler scale. The weight of the water (at 22°C) displaced by the eggs was determined by submerging the eggs in a beaker water on the same tared scale (Valkonen et al 2008). Egg specific gravity was then determined using the equation:
Specific gravity = Egg weight in air/displaced water weight
Haugh Units : Individual Haugh Unit (HU) score was calculated using the egg weight and albumen height (Haugh 1937). The Haugh Unit values was calculated for individual eggs using the following formula:
HU = 100 log10 (H + 7.5 – 1.7W0.37)
Where: H = Observed height of the albumen in mm
W = Weight of egg in grams
Egg yolk colour: Egg yolk colour was determined according to Roche yolk colour fan.
Yolk cholesterol was determined at 24, 38 and 60 weeks of age using the method of Fisher and Leiville (1957). The yolk and albumen of an egg boiled for 12-15 minutes were carefully separated. Two-gram yolk sample was placed in 50ml flask and extracted with chloroform-methanol (2:1) and filtered. The method of Zurkowski (1964) was then adopted for cholesterol analysis and it expressed as mg per dl of the yolk.
Table 3 shows the effects of rearing systems on the internal and external egg characteristics of 24 weeks old chickens (early production phase). The egg weight in grass pasture was higher than those of legume pasture and deep litter. The yolk weight in grass pasture was higher than that of the deep litter and legume pasture. The albumen weight also followed the same trend as that of the yolk weight. The egg shell thickness in LP and GP were similar but significantly higher than that of the DL. Furthermore, the yolk colour in LP and GP were similar and significantly deeper than that of DL. The specific gravity in DL and GP were similar but significantly lower than that of LP.
Table 4 shows the effects of rearing systems on the internal and external egg characteristics of 38 weeks old chickens (peak production phase). The egg weight recorded for the legume pasture was significantly higher than that of the deep litter. There was a similarity in egg length, egg width, and yolk height among the rearing systems. The yolk weight was higher in the legume pasture than that of the deep litter and grass pasture. Albumen weight in legume pasture and deep litter were similar but significantly lower than that of grass pasture. The height of albumen in DL and GP were similar but significantly lower than that of LP. The yolk colour in GP was similar to that of LP but significantly deeper than that of DL.
Table 5 shows the effects of rearing systems on the internal and external egg characteristics of 60 weeks old chickens (late production phase). The effect of rearing system on egg weight was similar in chickens on grass pasture and the deep litter. The weight of the eggs from the hens on legume pasture was however significantly higher than those of the grass and deep litter. The weight of the egg yolk was similar in the legume and grass pasture but significantly higher than that of the deep litter. The weight of albumen in the grass pasture was higher than those of the legume pasture and deep litter. Yolk height was significantly higher in LP than DL but was similar to that of GP. Shell thickness was significantly higher in GP than those of DL and LP but DL and LP were similar. Albumen index was similar in DL and GP but significantly lower than that of LP.
Table 3 : Effects of rearing systems on the Internal and external egg characteristics at 24 weeks old |
|||||
Qualities |
Rearing systems |
SEM |
P Value |
||
Deep litter |
Legume pasture |
Grass pasture |
|||
Egg weight (g) |
53.29b |
52.10c |
58.43a |
0.49 |
0.0001 |
Egg length (cm) |
5.11 |
5.13 |
5.28 |
0.05 |
0.29 |
Egg width (cm) |
4.07 |
4.05 |
4.13 |
0.02 |
0.13 |
Yolk weight (g) |
16.31b |
15.34c |
18.35a |
0.21 |
0.0001 |
Yolk height (cm) |
1.28 |
1.51 |
1.51 |
0.08 |
0.44 |
Albumen weight (g) |
33.19b |
32.20c |
33.98a |
0.18 |
0.0001 |
Albumen height (mm) |
4.82 |
5.27 |
5.13 |
0.095 |
0.14 |
Shell thickness (mm) |
0.38b |
0.47a |
0.47a |
0.01 |
0.0004 |
Yolk colour |
1.00b |
2.25a |
2.75a |
0.25 |
0.0005 |
Yolk index |
38.21 |
46.20 |
45.22 |
2.43 |
0.38 |
Egg shape index |
0.80 |
0.79 |
0.79 |
0.01 |
0.60 |
Albumen index |
20.37 |
20.85 |
18.78 |
0.93 |
0.67 |
Specific gravity |
1.12b |
1.21a |
1.12b |
0.02 |
0.02 |
Haugh unit |
66.86 |
71.41 |
68.03 |
0.95 |
0.12 |
ab: Means within rows with different superscripts are significantly different (P<0.05) |
Table 4: Effects of rearing systems on the Internal and external egg characteristics at 38 weeks old |
|||||
Qualities |
Rearing systems |
SEM |
P value |
||
Deep litter |
Legume pasture |
Grass pasture |
|||
Egg weight (g) |
59.07c |
61.14b |
64.35a |
0.47 |
0.0001 |
Egg length (cm) |
5.07 |
5.11 |
5.36 |
0.68 |
0.16 |
Egg width (cm) |
3.95 |
4.04 |
4.05 |
0.03 |
0.21 |
Yolk weight (g) |
17.70c |
18.37b |
18.89a |
0.12 |
0.0001 |
Yolk height (cm) |
1.68 |
1.69 |
1.64 |
0.04 |
0.68 |
Albumen weight (g) |
36.81b |
37.62b |
39.74a |
0.28 |
0.017 |
Albumen height(mm) |
4.28b |
5.14a |
4.15b |
0.16 |
0.0068 |
Shell thickness (mm) |
0.44 |
0.45 |
0.47 |
0.01 |
0.55 |
Yolk colour |
1.00b |
2.50a |
3.00a |
0.27 |
0.0001 |
Yolk index |
46.72 |
48.42 |
45.81 |
0.66 |
0.29 |
Egg shape index |
0.78 |
0.79 |
0.76 |
0.011 |
0.40 |
Albumen index |
17.39 |
18.11 |
15.17 |
0.65 |
0.16 |
Specific gravity |
1.16 |
1.13 |
1.10 |
0.013 |
0.12 |
Haugh unit |
63.14b |
69.93a |
59.01b |
1.669 |
0.0095 |
ab: Means within rows with different superscripts are significantly different (P<0.05) |
Table 5: Effects of rearing systems on the Internal and external egg characteristics at 60 weeks old |
|||||
Qualities |
Rearing systems |
SEM |
P Value |
||
Deep litter |
Legume pasture |
Grass pasture |
|||
Egg weight (g) |
63.74b |
66.21a |
64.71b |
0.28 |
0.0007 |
Egg length (cm) |
5.26 |
5.36 |
5.27 |
0.053 |
0.16 |
Egg width (cm) |
4.02 |
4.10 |
4.09 |
0.024 |
0.21 |
Yolk weight (g) |
18.71b |
19.43a |
19.66a |
0.11 |
0.0004 |
Yolk height (cm) |
1.49ab |
1.59a |
1.31b |
0.047 |
0.68 |
Albumen weight (g) |
39.36b |
40.88a |
38.80b |
0.23 |
0.0001 |
Albumen height (mm) |
4.90b |
5.50ab |
5.73a |
0.16 |
0.0068 |
Shell thickness (mm) |
0.38b |
0.47b |
0.58a |
0.03 |
0.54 |
Yolk colour |
1.00c |
2.25b |
3.00a |
0.26 |
0.0001 |
Yolk index |
44.23 |
45.04 |
40.27 |
1.15 |
0.28 |
Egg shape index |
0.76 |
0.77 |
0.78 |
0.0059 |
0.40 |
Albumen index |
19.59b |
25.66a |
22.07b |
0.86 |
0.16 |
Specific gravity |
1.17 |
1.12 |
1.25 |
0.034 |
0.12 |
Haugh unit |
67.11 |
71.42 |
73.42 |
1.41 |
0.0095 |
ab: Means within rows with different superscripts are significantly different (P<0.05) |
Table 6 shows the effects of rearing systems on the cholesterol content of eggs. The cholesterol level in DL was significantly higher than that of GP and LP. The level in LP was also lower than that of GP in the first laying phase. In the second laying phase, the level of cholesterol in DL was similar to that of GP but significantly higher than that of LP. DL recorded a higher (P<0.05) level of cholesterol in the third laying phase than those of LP and GP. The levels in LP and GP were similar.
Table 6: Effects of rearing systems on the cholesterol content of eggs |
||||||
Rearing systems |
SEM |
P Value |
||||
Parameters | Age |
Deep litter |
Legume pasture |
Grass pasture |
||
Cholesterol content |
24 weeks old |
540.25a |
516.63c |
528.62b |
2.19 |
<0.0001 |
(mg/dl) |
38 weeks old |
520.50a |
511.75b |
517.38ab |
1.71 |
0.10 |
60 weeks old |
528.25a |
511.12b |
518.00b |
2.36 |
0.0059 |
|
ab Means within rows with different superscripts are significantly different (P<0.05) |
The results from this study show that the weight of eggs in the pasture was higher than that of the deep litter in the early and peak phase. The higher egg weight may be due to the nutrients obtained from the plants in the free range which enhanced albumen deposition as Penz and Jensen (1991) reported that albumen deposition is greatly affected by the level of dietary protein. The increase in egg weight of the hens raised on pastures at the mid and late phase was is in agreement with the observation of Sencic et al (2006) who found that free range eggs were heavier than the other systems. This finding was also reported by Pavlovski et al (2004). The weights of eggs in legume pasture were smaller than those obtained in the grass pasture at the early laying phase. This may indicate superior ability of grass in enhancing deposition of albumen at this time.
The effect of rearing systems on egg shape index was not significant throughout this trial. This observation conforms to the findings of Sekeroglu et al (2010) who showed similar egg shape index for hens in deep litter and free range.
The colour of the yolk is determined by the presence and absence of xanthophylls some of which are precursor of vitamin A (Smith 1996). Therefore the colour of the yolk is influenced to a large degree by nutrition. As plants are major sources of xantophyl and carotenoids (Ponte et al 2004), dark yellow yolks can be produced by feeding laying birds on grass meal (Smith 1996). The hens housed in the free range in this trial produced eggs with deeper yolk colour than in the deep litter. This is in conformity with findings of Pavlovski et al (2004) who indicated that layers housed in free range system produced eggs with yolk of deeper yellow. Furthermore, Karadas et al (2005) showed that free-range hens have higher carotenoid levels in their eggs compared with intensively housed hens. Also, Sekeroglu et al (2010) reported that the yolk colour produced by the hens raised in the deep litter was lighter than those in free range.
Nys (2000) reported that there is a common association between yolk color and acceptability of eggs as a food and some consumers may prefer eggs with deeper yolk color. Eggs from the pasture had darker yolk than the ones from the deep litter and therefore might be preferred by consumers. In other word, this increases the marketability of the eggs produced by hens on the pasture.
The yolk color of eggs produced by the hens in the grass pasture was deeper than those in the legume pasture. This may indicate a higher level of carotenoid in the grass plant than in the legume.
Eggs with thick and strong shells are usually the most marketable (Melesse et al 2010). This trait is very important from economic point of view. The higher eggshell thickness of the grass-pastured chickens in this experiment could be an indication that calcium absorption and utilization was improved with consumption of forage plants. It could also be due to the ingestion of little stones from the ground and to the higher synthesis of vitamin D3 (Bar et al 1999) as a consequence of greater exposure to sunlight. It is well known that vitamin D is synthesized through a photochemical reaction requiring ultraviolet B photons (Wang et al 2001). The findings in this study is consistent with the observation of Aro et al (2009) who reported higher shell thickness with dietary inclusion of Cromolaena odorata leaf meal in the diet of layers. It is however at variance with the findings of Huque (1999) who reported that feeds scavenged by laying hens are deficient in protein and phosphorus. Another possible explanation to this is that thickness may be due to the fact that the hens had access to some additional nutrients in the soil. The higher egg shell thickness observed in the GP at 60 weeks old may be due to the age of the plant and the availability of the nutrients.
Albumen is a major determinant of internal egg quality. The higher albumen height and Haugh unit observed in the eggs of the hen on the pastures in this study indicates the superiority of the quality of the eggs. Also, lower albumen height in eggs from the deep litter may be partly due to their exposure to ammonia (from litter), which is known to affect albumen quality (Roberts 2004). This finding is however at variance with the findings of Sekeroglu et al (2010) who reported that there was no difference in the Haugh unit of the eggs from the hens on the deep litter and the free range. The Haugh unit observed in the eggs from the hens with access to legume pasture was higher than those with access to grass at the peak phase of egg production. This may suggest that some nutrients are available in the legumes at this period which enhanced the quality of the eggs. There is a dearth of information on the comparison of this parameter in legume and grass pasture.
The cholesterol concentration in eggs depends on the management and on nutrition (Förster and Flock 1997) and partly on synthesis of lipoproteins in the liver. The cholesterol content of eggs has become a very important quality criterion for consumers. The findings of this trial reveal higher cholesterol content in the eggs of the hens in the deep litter than the eggs from the hen on the pasture. This could partly be due the hypocholesterolemic effect of the forage plants. The lower cholesterol level in the free range eggs conforms to the findings of Wang et al (2009) who reported that the outdoor eggs had significantly lower yolk cholesterol concentration and whole egg content. The lower content of the cholesterol in the eggs from the pasture could also be attributed to more activities of the outdoor birds. It has been reported that cholesterol could be metabolized by many pathways. Most cholesterol are transported to yolk with very low density lipid, and for the others, some are transported to tissue to construct cells, some converted to cholesterol ramification, and some are digested in the intestines (Hargis 1988). The metabolism of the outdoor layers might be faster than those in the deep litter because of the frequent movement. It could therefore be speculated that more movement consumes more energy, and cell construction and digestion used more cholesterol than has been synthesized. Therefore, cholesterol level in yolk would be less in the outdoor egg than in deep litter. The level of cholesterol recorded for the eggs from grass-pasture chickens was higher than that of the legume pasture. This is in agreement with the observation of Karsten et al (2003).This indicates that legumes are superior in lowering egg cholesterol content.
The findings in this study clearly show that rearing layers birds with access to pasture enhanced egg quality parameters and that the type of pasture may influence the quantitative effect of the quality measure and timing of access during lay.
Rearing chicken with acces to pasture resulted in eggs with lower cholesterol content and greater shell thickness.
Anderson K E, Tharrington J B, Curtis P A and Jones F T 2004 Shell characteristics of eggs from historic strains of single comb white leghorn chickens and the relationship of egg shape to shell strength. International Journal of Poultry Science 3, 17-19.
Aro S O, Tewe O O and Aletor V A 2009 Potentials of Siam weed (Chromolaena odorata) leaf meal as egg yolk colourant for laying hens. Livestock Research for Rural Development. Volume 21, Article #171. http://www.lrrd.org/lrrd21/10/aro21171.htm.
Bar A, Vax E and Striem S 1999 Relationships among age, eggshell thickness and vitamin D metabolism and its expression in the laying hen. Comparative Biochemistry Physiology, 123:147-154.
Blokhuis H J 2004 Recent development in European and International welfare regulations. World’s Poultry Science Journal, 60: 469 – 477.
Doyon G M Bernier-Cardou R M G Hamilton F Castalgne and Randall C J 1986 Egg quality 2. Albumen quality of eggs from five commercial strains of white leghorn hens during one year of lay. Poultry Science, 65: 63-66.
Fisher H and Levelle G A 1957 Observation on the cholesterol, linoleic and linolenic acid content of eggs as influenced by dietary fats. Journal of Nutrition, 63: 119-129.
Förster A and Flock D K 1997 Egg quality criteria for table eggs and egg product. In: Proceedings of the VII European Symposium on the Quality of Eggs and Egg Products, Poznan, pp. 28–38.
Glatz P C, Ru Y J, Miao Z H, Wyatt S K and Rodda B J 2005 Integrating poultry into a crop and pasture farming system. International Journal of Poultry Science, 4: 187-191.
Hargis P S 1988 Modifying egg yolk cholesterol in the domesticfowl – A review. World’s Poultry Science Journal, 44:17–29.
Haugh R R 1937 The haugh unit for measuring egg quality. US Egg Poultry Magazine, 43: 552-555.
Huque Q M E 1999 Nutritional status of family poultry in Bangladesh. Livestock Research for Rural Development. 11(3): http://www.cipav.org.co/rrd/ rrd11//uq13.htm
Karadas F, Wood N A R, Surai P F and Sparks N H C 2005 Tissue-specific distribution of carotenoids and vitamin E in tissues of newly hatched chicks from various avian species. Comparative Biochemistry Physiology A. 140:506–511. http://www.ncbi.nlm.nih.gov/pubmed/15936711.
Karsten H D, Crews G L, Stout R C and Patterson P H 2003 The impact of outdoor coop housing and forage based diets vs. cage housing and mash diets on hen performance, egg composition and quality. International Poultry Scientific Forum. ABS. Atlanta, Georgia.
Karsten H P, Patterson Stout R and Crews G 2010. Vitamins A, E, and fatty acid composition of the eggs of caged hens and pastured hens. Renewable Agriculture and Food System, 25: 45-54.
Leyendecker M, Hamann H, Hartung J, Kamphues J, Ring C, Glunder G, Ahlers C, Sander I, Neumann U and Dist O 2001 Analysis of genotype environment interactions between layer lines and hen housing systems for performance traits, egg quality and bone breaking strength. 2nd communication: egg quality traits. Zuchtungskunde, 73:308-323
Melesse A, Maak S and von Lengerken G 2010 Effect of long-term heat stress on egg quality traits of Ethiopian naked neck chickens and their F1 crosses with Lohmann White and New Hampshire chicken breeds. Livestock Research for Rural Development. Vol. 22, Article #71. http://www.lrrd.org/lrrd22/4/mele22071.htm.
Nworgu F C, Oduola O A, Alikwe P C and Ojo S J 2012 Effects of basil (Ocimum gratissimum) leaf supplement on initiation of egg laying and egg quality parameters of growing pullets. Journal of Food Agriculture and Environment, 10: 337-342.
Nys Z 2000 Dietary carotenoids and egg yolk coloration- a review. Arch Geglugelkd, 64:45- 54.
Pavlovski Z, Skrbic Z and Lukic M 2004 Effect of housing system on egg quality traits in small layers flocks. Proceeding of the 22th World`s Poultry Congress, June 8-13, Istanbul-Turkey, pp: 357-357.
Penz A M and Jensen L S 1991 Influence of protein concentration, amino acid supplementation, and daily time to access to high- or low-protein diets on egg weight and components in laying hens. Poultry Science, 70: 2460-2466.
Ponte P I P, Ferreria L M A, Soares M A C, Aguiar M A N, Lemos J P Mendes I and Fontes C M G A 2004 Use of cellulases and xylanases to supplement diets containing alfalfa for broiler chicks: effects on bird performance and skin colour. Jounal of Applied Poultry Research, 13: 412-420.
Roberts J R 2004 Factors affecting egg internal quality and egg shell quality in laying hens. Journal of Poultry Science, 41:161-177.
Sekeroglu A, Musa S, Ergun D, Zafer U, Muammer T, Mustafa S and Hussain O 2010 Effects of Different Housing Systems on Some Performance Traits and Egg Qualities of Laying Hens. Journal of Animal Veterinary Advances, 9 : 1739-1744.
Sencic D, Antunovic Z, Domacinovi M, Speranda M and Steiner Z 2006 Egg quality from free range and cage system of keeping layers. Stocarstvo, 60: 173 – 179.
Simopoulos A P and Salem N 1992 Egg yolk as a source of long-chain polyunsaturated fatty acids in infant feeding. American Journal of Clinical Nutrition, 55: 411-414.
Smith A J 1996 Poultry. Macmillan Education Ltd, London and Oxford. pp.130.
Sun T Z, Liu L and Long R 2012 Aspects of lipid oxidation of meat from free-range broilers consuming a diet containing grasshoppers on alpine steppe of the Tibetan Plateau. Poultry Science, 91: 224-231.
Torges H G, Matthes S and Harnish S 1976. Environmental effects on egg quality. In: Egg Quality – Current Problems and Recent Advances, Ed. Butterworths, U.K., pp.219-234.
Valkonen E, Venäläinen E, Rossow L and Valaja J 2008 Effects of Dietary Energy Content on the Performance of Laying Hens in Furnished and Conventional Cages. Poultry Science, 87 (5): 844-852.
Wang T, Bengtsson G, Kärnefel T and Björn L O 2001 Provitamin and vitamin D2 in Cladina spp. over a latitudinal gradient: possible correlation with UV levels. Journal of Photochemistry Photobiology B. 62: 118-122.
Wang X L, Zheng J X, Ning Z H, Qu L J, Xu G Y and N Yang N 2009 V Laying performance and egg quality of blue-shelled by different housing systems. Poultry Science, 88 :1485–1492.
Zurkowski P 1964 A rapid method for cholesterol determination with a single reagent. Clinical Chemistry 10: 451-455.
Received 25 September 2014; Accepted 18 October 2014; Published 3 November 2014