1. Introduction
From stand-alone meals to further processed foods and baking, eggs are a staple of the American diet. The United States alone produces almost 98 billion eggs a year [
1]. The majority of these eggs are produced in the conventional battery cage laying system; however, the number of cage-free facilities is on the rise [
2,
3,
4,
5,
6]. Driven by both consumer interest groups and legislation, many regions of the United States have outright banned the use and sale of eggs from battery cages [
7,
8]. Due to these regulations, many groceries, food services and restaurants have pledged to discontinue the use of eggs from caged environments in favor of eggs from alternative environments such as cage-free and colony cages [
9,
10,
11,
12,
13,
14,
15]. Unfortunately, this will lead to higher costs, which will ultimately be passed to consumers who may not be willing to pay the increased cost if given the option [
16,
17,
18]. Therefore, it is important to understand how these environments affect the quality of the eggs that are produced since egg quality can affect the end product [
19].
Physical egg quality parameters may affect the quality and consumer perceptions of table eggs and, potentially, the egg products derived from them. These parameters usually include shell and vitelline membrane strength, shell color, Haugh unit, yolk color and dry egg mass. Shell strength and elasticity directly affect the chance of breakage during processing and transportation. Furthermore, eggs with stronger shells can break cleaner at the breaker plant. The vitelline membrane is important in keeping the yolk separate from the albumen. This is important as consumers prefer their yolks to remain unbroken during cooking, and strong membranes keep the yolk and albumen separate during further processing and separating. Egg weight is directly correlated to marketable egg sizes and the amount of material for further processing. Albumen height, as well as Haugh units, directly correlate to the internal egg quality (and grades) of the eggs. Both shell and yolk color are important in consumer perceptions of table eggs. Finally, whole egg solids are the amount of dry egg matter in the egg, which is important for further processing.
Interestingly, the majority of research on how the housing environment affects egg quality has been performed on brown egg layers, as seen by Pires et al.’s review paper [
20]. While both brown and white egg layers are laying hens, these types of chickens are vastly different and present different egg quality parameters [
21,
22,
23,
24,
25,
26]. Therefore, there is a need for more information regarding how the housing environment affects the quality of eggs produced by white egg layers. Some studies indicate that the housing environment does not affect white egg layers [
23,
24,
27,
28,
29]. However, there are a few studies that identify better egg quality parameters in intensive environments, such as conventional battery cages [
21,
30,
31]. Even so, some studies also indicate that floor pens provide an optimal environment for white egg layers [
21]. Furthermore, researchers have indicated the importance of performing similar studies across regions to avoid confounding factors such as diet, environmental and management differences [
32]. Therefore, the objective of this study was to evaluate the effect of the housing environment on egg quality from modern white egg layer strains using standard North American management practices and nutrition. Based on previous research, we hypothesize that the housing environment will have no effect on the physical quality of white eggs.
4. Discussion
The housing environment was found to have an effect on several egg quality parameters. While extensive research has been performed using brown egg layers to compare housing environments, there is limited research related to white egg layers [
26]. Furthermore, researchers have demonstrated major differences between brown and white egg layer performance and egg quality. [
21,
22,
23,
24,
25]. Therefore, brown egg layer studies would not be applicable for comparison against white egg layers as physical egg quality parameters between white and brown egg layers are very different [
21,
22,
25,
26].
The housing environment influenced several egg quality traits. Starting with shell color using reflectivity, the housing environment had an effect on shell color only at the end of the study, where cage-free hens had the lightest eggs. Nutrient recycling in the extensive systems may have caused these color variations. When looking at shell reflectivity, it is important to note that a pure white egg will have a reflectivity of 83.3%. Consumers prefer eggshells closest to this 83.3% reflectivity as consumers prefer white eggs to be as white as possible [
40]. Unfortunately, it is not yet understood what level of difference in shell reflectance consumers can perceive in eggshells. Interestingly, the present study seems to be unique in its measurement of shell reflectivity in white egg layers. Many studies evaluate brown egg color and reflectivity in relation to the housing environment; however, it seems that studies evaluating egg quality of white egg layers in various housing environments lack measurement of shell color or reflectivity [
41,
42,
43].
Overall, we identified that CF eggshells were stronger than eggshells from both colony cages. Interestingly, at the first sampling date, CC eggshells were stronger than colony cage eggshells, and at weeks 51 and 63, CF eggshells became stronger than other environments. We did not identify any differences in eggshell elasticity between treatments. Stronger eggshells are more desirable by consumers, producers and further processors [
44,
45]. Eggs that have stronger shells tend to break less during transportation [
44,
45]. Philippe et al. [
29] and de Oliveria et al. [
46] found no difference between ECS and CC systems, which confirms the findings of the present study. Hidalgo et al. [
30] found CF eggs at the grocers had weaker shells than their caged counterparts, although the authors did not identify the egg color of the eggs chosen. Eggshell strength can be dependent on several aspects of the egg. While shell thickness was not measured for this study, it can be hypothesized that the weaker eggs could have had thinner eggshells. Research has also indicated that differences in eggshell-breaking strength may be caused by differences in eggshell mineral content, which should be further investigated in a subsequent study [
47]. Furthermore, it is well known that chickens will practice coprophagic behaviors, thereby potentially consuming extra minerals and vitamins [
48,
49,
50]. Therefore, we also hypothesize that CF hens reabsorbed vitamins and minerals through their feces by this behavior which caged hens would not have the ability to do.
Haugh unit is a measure of the internal freshness of the egg and is a function of egg weight and albumen height [
37]. Higher Haugh units are correlated with superior internal egg quality [
37]. Haugh unit has also been shown to be directly related to internal egg grades as well (USDA AA, A, and B internal grades) [
51]. The present study found overall effects on albumen height, egg weight, and Haugh unit. In general, eggs from conventional cages had higher egg weights and Haugh units, while eggs from the cage-free environment had lower egg weights and Haugh units. Furthermore, while the Haugh unit was not affected, the ECS environment had smaller eggs and lower albumen than the other environments as well. We also saw differences overall and no differences in the individual weeks between environments when looking at the Haugh unit and egg weight. This could be due to the larger sample size, as the overall calculation was based on all of the data, shrinking the overall standard error. Several other studies confirm our findings, such as Singh et al. [
21], who found that caged eggs had higher albumens than cage-free eggs, Sharma et al. [
24] and Philippe et al. [
29] found no difference in Haugh Unit between ECS and CS environments. However, Barbosa Filho et al. [
28] found no difference in egg quality between caged and cage-free hens. Singh et al. [
21], Barbosa Filho et al. [
28] and Al-Awadi et al. [
52] also found no significant difference in egg weight between caged and cage-free eggs, which disagrees with our findings. These differences could be due to the strain utilized, as the most modern study from this group is almost 20 years old, and the genetics of the laying hen has improved greatly since then [
53]. Sharma et al. [
24] and Philippe et al. [
29] found no difference between both types of colony cages, which is in agreement with our findings.
Yolk color, measured by the DSM color fan, was affected by the housing environment. Yolk color is important as darker yolks are typically regarded as superior across the globe [
54]. Eggs from the CF environment exhibited darker yolks than eggs from other environments. Furthermore, adding enrichments to the colony cages did not affect the yolk color. These results are consistent with Singh et al. [
21], who discovered that CF eggs had darker yolks than CC eggs, and Philippe et al. [
29], who found no difference between colony cages. However, these results are also inconsistent with Hidalgo et al. [
30], who found lighter yolks in CF eggs. Yolk color is typically highly affected by the feed that the hens consume; however, in this study, there was no difference in the feed between treatments. Philippe et al. [
29] found that in aviaries, which had access to litter substrates, the hens had darker yolks. Philippe et al. [
29] also hypothesized that the yolks were darker due to the litter that the hens may have consumed. Furthermore, according to Singh et al. [
21], high egg production can negatively influence yolk color, which may be the case for the present study as well. Therefore, in future research, yolk, liver and fat pad carotenoid levels should be measured, and behavior analysis could also identify litter-eating behaviors as well.
The housing environment was found not to affect vitelline membrane strength (except for week eighty-seven, where CF eggs had stronger membranes) or elasticity. Consumers and further processors prefer stronger vitelline membranes [
55]. Consumers prefer the yolk and the albumen to be separate during some cooking activities [
55]. Moreover, further processors prefer the yolk to stay intact when separating from albumen, as small amounts of yolk can reduce the functional properties of the albumen leading to financial losses [
55]. Measuring the housing environment’s effect on vitelline membrane parameters of white eggs appears to be a novel contribution of this study as most current research lacks this information. However, in a study performed by Jones et al. [
56], CF white eggs purchased in a grocery store showed weaker vitelline membranes than conventional caged eggs, although these eggs had the oldest retail age. While this study did not show any differences in vitelline membrane properties, further research in housing environments and vitelline membrane characteristics will need to be performed to confirm these findings.
Finally, this study found that CF eggs had a greater amount of egg dry matter than ECS eggs overall. Egg dry matter percentage is important for further processing as it directly corresponds to the amount of dry product that can be produced per egg. This can directly affect the profitability of further processed eggs as a higher solids percentage yields more dry egg product when further processed [
57]. Hidalgo et al. [
30] found no difference between CC and CF egg dry matter percentage, which agrees with the findings of the present study. Philippe et al. [
29] found that CS and ECS eggs did not differ in their dry matter percentage, which confirms the findings of this study.