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Effect of a commercial housing system on egg quality during extended storage1
Effect of a commercial housing system on egg quality during extended storage1 D. R. Jones,*2 D. M. Karcher,† and Z. Abdo‡ *Egg Safety and Quality Research Unit, USDA Agricultural Research Service, Athens, GA 30605; †Department of Animal Science, Michigan State University, East Lansing 48824; and ‡South Atlantic Area, USDA Agricultural Research Service, Athens, GA 30605 < 0.05) were significantly greater for conventional cage than enriched eggs. Static compression shell strength was greatest (P < 0.05) for enriched eggs compared with aviary. No overall housing system effects for yolk measurements, shell dynamic stiffness, or whole egg total solids were observed. Albumen height, Haugh unit, and yolk quality measurements were all greatest at 0 and lowest at 12 wk of storage (P < 0.05). The rate of quality change among the housing systems for each measured attribute at 4, 6, and 12 wk was determined. Other than differences in the change of egg weight at 4 wk, no significant differences in the rate of quality decline were found among the housing systems. The results of the current study indicate that current US egg quality standards should effectively define quality for commercially produced conventional cage, enriched colony cage, and cage-free aviary eggs.
Key words: sustainable, egg production, housing, egg quality, storage 2014 Poultry Science 93:1282–1288 http://dx.doi.org/10.3382/ps.2013-03631
INTRODUCTION The US egg industry has expanded to offer a variety of purchasing options to consumers. This expansion has occurred due to market demands and legislative actions defining animal confinement parameters. Traditionally, laying hens in the United States have been housed in conventional cages. A great deal is known on the effects of conventional cages on egg production, egg quality, and egg safety. A volume of research has examined the effect of alternative housing systems on egg quality and safety in the European Union (Abrahamsson and Tauson, 1998; Wall and Tauson, 2002; Guesdon
©2014 Poultry Science Association Inc. Received September 18, 2013. Accepted November 29, 2013. 1 Research support provided in part by a grant from the Coalition for a Sustainable Egg Supply (Kansas City, MO). 2 Corresponding author: [email protected]
and Faure, 2004; Van Den Brand et al., 2004; Vits et al., 2005; Hidalgo et al., 2008; De Reu et al., 2009; Wall, 2011). Unfortunately, many of the outcomes cannot be directly transferred to United States alternative housing systems due to substantial differences in hen management, hen genetics, and egg holding methods between the United States and European Union (Holt et al., 2011). Controlled production studies provide a clearer understanding of the effects of housing systems on egg production and quality (Anderson, 2012). Under such conditions, hens in each housing system are provided identical nutrition, controlled lighting, and other management considerations. Commercial hen production studies provide a real world perspective, as hens are managed in an appropriate manner to maximize economic impact. Commercial studies relinquish scientific control of hen management, yet provide invaluable information on commercial application of housing systems.
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ABSTRACT Egg producers in the United States are utilizing a variety of commercial egg production systems to provide consumer choice and meet legislative requirements. Consumer egg grades in the United States were developed for conventional cage production, and it is unclear what effect alternative production systems might have on egg quality during retail and consumer home storage. The current study was undertaken to determine what changes in egg quality characteristics occur during extended cold storage for commercially produced conventional cage, enriched colony cage, and cage-free aviary eggs. During 12 wk of cold storage, egg weight, albumen height, Haugh unit, static compression shell strength, vitelline membrane strength and deformation, yolk index, shell dynamic stiffness, and whole egg total solids were monitored. Overall, aviary and enriched eggs were significantly (P < 0.05) heavier than conventional cage. Albumen height and Haugh unit (P
HOUSING SYSTEM AND EGG QUALITY DURING STORAGE
MATERIALS AND METHODS Pullets The experimental protocol was approved by the Michigan State University Institutional Animal Care and Use Committee. Lohmann White laying hens were housed at a commercial egg facility located in the Midwest United States. The pullets were housed in conventional cages or cage-free aviary (aviary) rearing systems. Pullets in the conventional cages were provided 247.74 cm2 (38.4 in2) with 15 birds per cage. Pullets had access to 4.06 cm (1.6 in) of feeder space per bird with 7.5 birds per nipple water. The aviary rearing system had 218 birds per cage with 159.94 cm2 (24.79 in2) of cage space, 2.18 cm (0.86 in) of perch space, and 4.37 cm (1.72 in) of feeder space per bird with 11 birds per nipple water from 0 to 9 wk of age. From 9 to 18 wk, the pullets had additional cage space provided, increasing the total cage space available by 248.97 cm2 (38.59 in2) and 1.09 cm (0.43 in) of perch space. Seven additional nipple waters resulted in 8 birds per nipple. The pullets also had floor access from 6 to 18 wk, providing 100.13 cm2 (15.52 in2) per bird. The pullets were housed at 19 wk of age in 3 different housing systems (conventional cage, aviary, and enriched colony cage) and depopulated at 77 wk of age.
Housing Systems Conventional Cage. The conventional cage house was a belted, preexisting commercial house with a hen population of 193,424. The conventional house consisted of 10 rows of conventional cages with 8 tiers and a walkway between tiers 4 and 5. The conventional cage provided 567.75 cm2 (88 in2) per bird with 6 birds per
cage. Each conventional cage provided 10.16 cm (4 in) of feeder space per bird and 6 hens per nipple water. The house was tunnel ventilated and had manure removed every 3 to 4 d. Enriched Colony Cage. The enriched colony house was a belted, newly built facility housing 46,795 laying hens. The facility consisted of 5 rows of colony cages with 4 tiers per row. Each enriched colony cage contained 60 birds that provided 753.22 cm2 (116.75 in2) of physical space. Each colony cage provided several amenities (expressed on a per bird basis), including 12.07 cm (4.75 in) of feeder space, 17.73 cm (6.98 in) of perch space, 63.03 cm2 (9.77 in2) of nest space, 26.52 cm2 (4.11 in2) of scratch pad space, and 7.5 birds per water line nipple with drip cup. The house had ceiling inlets and was cross-ventilated with manure removal every 3 to 4 d. Cage-Free Aviary. The cage-free aviary system (aviary) was ventilated the same as the enriched colony system and was a newly built facility housing 49,842 laying hens. The aviary had 6 rows of housing, with litter access on the bird side and a human aisle on the opposite side. The row length was divided by wire partitions that created 10 compartments of laying hens. The population size consisted of 852 laying hens per compartment along the 2 exterior sides of the facility and 1,704 laying hens per compartment in the 2 interior rows. This provided each hen in the exterior compartments with 1,170.71 cm2 (181.46 in2) and interior compartments with 1,166.45 cm2 (180.80 in2) of total area. The area was calculated within the aviary system as 547.03 cm2 (84.79 in2) of cage wire space and 103.61 cm2 (16.06 in2) of solid surface plates; for exterior compartment floor access, 319.35 cm2 (49.50 in2) under the aviary and 200.71 cm2 (31.11 in2) in front of the aviary; and for interior compartment floor access, 319.35 cm2 (49.50 in2) under the aviary and 196.39 cm2 (30.44 in2) in front of the aviary. Irrespective of compartment location, hens had access to 10.19 cm (4.01 in) of feeder space, 15.24 cm (6 in) of perch space [11.86 cm (4.67 in) inside the housing system and 3.38 cm (1.33 in) in the forage area], 86.32 cm2 (13.38 in2) of nest space area, and 8.9 birds per nipple water.
Lighting and Diet The 3 housing systems were located on a single farm and experienced identical seasonal temperature fluctuations. The photoperiod at time of lay was 16L:8D with a light intensity of 10 lx. Laying hens had ad libitum access to water and were fed commercially available diets formulated to maximize production efficiency. The cage-free aviary feeding schedule consisted of 5 feedings a day for 16 min each. The enriched colony and conventional cage had 2 feedings a day for 16 min each, with the scratch augers in the enriched colony running at the same time as a feeding for 30 s.
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Egg quality declines as an egg ages (Silversides and Villeneuve, 1994; Jones et al., 2002, 2010; Jones and Musgrove, 2005; Biladeau and Keener, 2009). Defined quality parameters exist for eggs marketed in the United States (USDA, 2000) specifying egg grades. Each state in the United States has a defined period of time eggs can be marketed in retail, usually 30 or 45 d postprocessing. During this time, eggs must maintain the quality grade standards (USDA, 2000) identified on the carton (generally grade A). Egg processing guidelines (USDA, 2008) and quality standards in the United States are based on conventional cage egg production. It is unknown if current US egg guidelines and standards are appropriate for ensuring the quality and safety of eggs produced from commercial alternative production systems. The current study was undertaken to determine the effect of commercial conventional cage, enriched colony cage, and cage-free aviary (aviary) egg production on various egg quality factors during extended cold storage.
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Egg Processing and Storage
Egg Quality Assessments Each sample time, 12 to 18 eggs per treatment were screened via candling to remove cracked eggs before egg quality assessments were conducted. The number of eggs examined for each treatment was dependent on the total number of intact eggs received per treatment during egg replicate shipment. Eggs were removed from cold storage immediately before egg quality assessments were conducted to ensure comparable egg temperatures. Egg temperature was monitored throughout quality assessments and ranged between 7 to 9°C. Egg quality measurements were tracked for individual eggs with the exception of whole egg solids, which were conducted on pools. Each egg was assessed 3 times for shell dynamic stiffness on an acoustical egg tester (KU Leuven, Leuven, Belgium) as described by De Ketelaere et al. (2002). Individual egg weights were recorded with a TSS QCD system (Technical Services and Supplies, Dunnington, York, United Kingdom). Shell static compression strength was measured with a texture analyzer (TA-XT2plus; Texture Technologies, Scarsdale, NY) equipped with a 5-kg load cell and 3-in. diameter aluminum compressions disc (TA-30, Texture Technologies). The egg was presented on its side in an egg holder with posts (TA-650, Texture Technologies). A test speed of 2 mm/s and a trigger force of 0.001 kg were used. Albumen height and Haugh unit (Haugh, 1937) were recorded with the TSS QCD system. Yolk index was determined by measuring yolk height with a tripod micrometer (S-6428; B.C. Ames Inc., Melrose, MA) and yolk width with a digital micrometer (Thermo Fisher Scientific, Waltham, MA). The yolk was separated from albumen before vitelline membrane strength and deformation were measured with a texture analyzer (TA-XT2plus; Texture Technologies) according to the procedures of Jones et al. (2010). The albumen and
Statistical Analysis Data collected during the study were subjected to an ANOVA utilizing the PROC GLM analysis in SAS (SAS Institute, 2002). Housing system and week of storage were the main effects. The decline in egg quality during storage was determined for each parameter monitored in the study at 4 (28 d), 6 (42 d), and 12 wk (84 d) and compared between housing systems. The time points for egg quality decline analysis were selected based on individual US state allowances for eggs to be marketed (generally 30 or 45 d) and also to account for in-home consumer storage. The average change in each egg quality measurement for a housing system between 0 wk and the set sample times was calculated for each egg storage set replicate. The rate of quality decline was then analyzed using the ANOVA as implemented within PROC GLM to determine if housing system differences existed.
RESULTS AND DISCUSSION The average values for all monitored egg quality indicators throughout the 12 wk of cold storage are presented in Table 1. Eggs from the aviary and enriched systems were heavier than those from conventional cages (58.69 and 58.88 vs. 57.97 g; P < 0.05). Though the difference was significant, less than a gram of difference in average egg weight was found between the systems. Albumen height and Haugh unit were greater (5.81 mm and 74.61, respectively; P < 0.05) for conventional cage eggs compared with those from the enriched system. Static compression shell strength was greater (P < 0.05) for enriched system eggs (39.57 N) than aviary (38.53 N). No significant differences were observed between housing treatments for average values of vitelline membrane strength, vitelline membrane deformation (elasticity), yolk index, shell dynamic stiffness, or whole egg percent total solids. The combined egg quality values for all treatments during each week of storage are presented in Table 2. Overall, egg weight did not significantly change during 12 wk of cold storage. Albumen height and Haugh unit decreased (P < 0.05) throughout storage, with the highest values (7.21 mm and 84.62, respectively) occurring at 0 wk and lowest values (4.80 mm and 66.21, respectively) measured at 12 wk. A lower (P < 0.05) static compression shell strength was found at 8 wk of storage compared with all other monitoring times. Vitelline membrane strength and deformation decreased throughout storage (P < 0.05), with the greatest levels (1.77 N and 7.84 mm, respectively) detected at 0 wk and lowest levels (1.17 N and 6.17 mm, respectively)
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Eggs were collected from each housing system on 4 occasions (hen age 26, 41, 57, and 70 wk) and shipped to the laboratory overnight. Immediately upon arrival, eggs were washed with a pilot egg washer under recommended USDA guidelines (USDA, 2008) according to the procedures described by Jones et al. (2005). The pilot egg washer had been modified to contain 60 eggs per wash cycle and commercial egg wash detergent was used (Exalt II; Zee Company Inc., Chattanooga, TN). After washing and drying procedures were complete, eggs were placed in clean foam cartons (Dolco Packaging, Decatur, IN) and stored at 4°C for the remainder of the study. Eggs were allowed to equilibrate to the refrigerated temperature overnight before conducting 0 wk assessments due to egg temperature effects on egg quality measurements (Keener et al., 2006). Subsequent egg testing was conducted every other week through 12 wk of storage.
yolk from 3 eggs were combined to form 4 to 6 pools per treatment (dependent on replicate). Whole egg total solids were determined according to the procedures of Jones et al. (2010). Triplicate measurements were made per pool.
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HOUSING SYSTEM AND EGG QUALITY DURING STORAGE Table 1. Effect of housing system on average values for egg quality indicators throughout 12 wk of cold storage
Housing system
Egg weight (g)
Albumen height (mm)
Aviary Conventional cage Enriched colony cage SE
58.69a 57.97b 58.88a 0.25
5.68b 5.81a 5.57b 0.05
a,bMeans
Haugh unit
Shell strength (N)
Vitelline membrane strength (N)
Vitelline membrane deformation (mm)
73.58ab 74.61a 72.60b 0.43
38.53b 39.36ab 39.57a 0.30
1.45 1.40 1.40 0.03
7.00 6.85 6.81 0.06
Yolk index
Shell dynamic stiffness1 (kN/m)
Whole egg total solids1 (%)
0.47 0.48 0.47 0.01
158.68 159.93 159.95 0.58
23.23 23.13 23.20 0.03
within a column with different letters are significantly different (P < 0.05). housing system × egg storage interaction (P < 0.05).
1Significant
2 g heavier than at 0 wk, whereas aviary and enriched eggs weighed less than 0 wk eggs from those systems (−0.27 and −1.88 g, respectively). The differences in change in egg weight between housing systems during the first 4 wk of storage could be due to variability within housing systems on the size of eggs being produced. Additionally, eggs were randomly selected for each monitoring period and conventional cage eggs at 4 wk of storage during the fourth replicate of the study were heavier than the 0-wk eggs. Otherwise, no differences were noted in the rate of decline for any egg quality parameters measured between the housing systems at 4, 6, and 12 wk of storage. In the current study, egg weights were significantly greater for aviary and enriched cages compared with conventional cage production. This differs from Guesdon and Faure (2004), who reported no difference in egg weights between conventional and enriched cages. Jones et al. (2010) found egg weight during 5 wk of cold storage to be highly variable, which agrees with the current study when considering the rate of egg weight changes during storage for the 3 housing systems. Additionally, in the current study, no differences were observed in average egg weights compared between storage weeks when all housing systems were combined. Jones and Musgrove (2005) also reported fairly consistent egg weights during 10 wk of cold storage. Albumen height and Haugh unit values decreased during storage in the current study, which concurs with the findings of others (Jones et al., 2002, 2005, 2010; Biladeau and Keener, 2009). Overall, albumen height and
Table 2. Effect of extended cold storage on egg quality indicators
Item Egg storage (wk) 0 2 4 6 8 10 12 SE a–fMeans
Egg weight (g)
Albumen height (mm)
58.41 58.22 58.47 58.64 58.60 58.57 58.68 0.38
7.21a 6.21b 5.64c 5.64c 5.17d 5.13d 4.80e 0.07
Haugh unit
Shell strength (N)
Vitelline membrane strength (N)
Vitelline membrane deformation (mm)
84.62a 78.24b 73.69c 73.72c 69.54d 69.16d 66.21e 0.68
39.47a 39.18a 39.21a 40.12a 37.58b 39.51a 39.02a 0.46
1.77a 1.52b 1.50bc 1.39cd 1.32de 1.25ef 1.17f 0.04
7.84a 7.11b 7.15b 6.84c 6.56d 6.54d 6.17e 0.10
within a column with different letters are significantly different (P < 0.05). housing system × egg storage interaction (P < 0.05).
1Significant
Yolk index
Shell dynamic stiffness1 (kN/m)
Whole egg total solids1 (%)
0.49a 0.48b 0.48b 0.47bc 0.47bc 0.47bc 0.46c 0.01
157.31 159.34 160.39 160.44 158.80 159.10 161.25 0.91
23.00 23.15 23.05 23.18 23.17 23.39 23.38 0.05
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found at 12 wk. Average yolk index decreased (P < 0.05) throughout storage, ranging from 0.49 to 0.46. A significant housing system × egg storage interaction was found for shell dynamic stiffness (Figure 1) and whole egg total solids (Figure 2). Figure 1 illustrates how eggs from each housing system had different shell dynamic stiffness properties throughout storage. Conventional cage-produced eggs had an increase in shell dynamic stiffness between 0 and 2 wk, which remained fairly constant throughout the remaining sampling periods. Eggs from aviary production had a general increase in shell dynamic stiffness throughout the storage period. Conversely, eggs from enriched production had a general decrease in shell dynamic stiffness throughout the 12 wk of storage. Whole egg total solids generally increased for each housing system through the 12-wk storage period (Figure 2), but the rate of increase was variable for the 3 housing systems, resulting in a housing system × egg storage interaction (P < 0.05). The rate of change at 4, 6, and 12 wk (28, 42, and 84 d) of cold storage, compared with 0 wk values, for each of the monitored egg quality characteristics is presented in Table 3. Comparisons in the rate of change in egg quality were conducted at these points to discern if housing system affected the ability of eggs in retail to meet USDA grade standards for common use by or sale by dates (30 or 45 d postprocessing) and also after storing in consumer refrigerators for an extended period (12 wk). The only occurrence of significance between housing systems was for the change in egg weight at 4 wk, when conventional cage eggs were approximately
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Figure 2. Interaction of housing system × egg storage on whole egg total solids (P < 0.05).
Haugh unit were greater for conventional cage- than enriched cage-produced eggs. Singh et al. (2009) reported greater albumen heights in conventional cage eggs compared with floor hens. Vits et al. (2005) found significant differences between enriched housing systems for Haugh unit scores. Conversely, Wang et al. (2009) found no difference in the average albumen height and Haugh unit values from conventional cage and outdoor production systems. Additionally, Varguez-Montero et al. (2012) found no differences in albumen height and Haugh unit when comparing conventional cage, outdoor, and indoor production systems and Hidalgo et al. (2008) found similar Haugh unit values in Italian retail eggs from free range, cage, and barn production. Whereas the overall albumen height and Haugh unit values were found to be different between conventional and enriched colony cage production in the current study, the rate of decline at 4, 6, and 12 wk of storage
for the 2 parameters was never significantly different between any of the housing systems. No differences were found in overall vitelline membrane strength or elasticity between the housing systems. Previously, vitelline membrane characteristics had not been extensively compared between hen housing systems. When all eggs monitored during the study were considered, vitelline membrane strength and elasticity significantly decreased during extended cold storage. Previous research also found vitelline membrane strength to decrease with increased egg age (Funk, 1944; Fromm and Matrone, 1962; Oosterwoud, 1987; Jones et al., 2002, 2010). Conversely, Jones et al. (2005) and Biladeau and Keener (2009) found no difference in vitelline membrane strength during prolonged storage. In both cases, vitelline membrane strength measurements were assessed via static compression (as was the case in the current study), utilizing approximately
Table 3. Effect of housing system on changes in egg quality factors at 4, 6, and 12 wk of cold storage compared with initial values Egg weight (g)
Housing system 4 wk Aviary Conventional cage Enriched colony cage SE 6 wk Aviary Conventional cage Enriched colony cage SE 12 wk Aviary Conventional cage Enriched colony cage SE a,bMeans
−0.27b 2.09a −1.88b 0.70 −0.04 2.11 −1.47 0.91 −0.74 1.42 −1.22 0.76
Albumen height (mm)
−1.57 −1.62 −1.60 0.38 −1.35 −1.46 −1.89 0.27 −2.23 −2.48 −2.43 0.41
Haugh unit
−11.21 −11.49 −11.16 3.05 −9.75 −10.21 −13.06 1.79 −16.44 −20.24 −18.74 3.77
Vitelline membrane strength (N)
Shell strength (N)
−0.81 1.06 −0.58 1.53 0.54 0.68 0.50 1.81 −1.09 1.38 −1.43 1.70
−0.26 −0.12 −0.34 0.09 −0.42 −0.20 −0.43 0.12 −0.64 −0.40 −0.61 0.15
Vitelline membrane deformation (mm)
−0.64 −0.27 −0.96 0.28 −1.25 −0.53 −1.10 0.22 −1.87 −1.20 −1.80 0.37
in a column, within an egg age period, with different letters are significantly different (P < 0.05).
Shell dynamic stiffness (kN/m)
Yolk index
−0.01 −0.01 −0.02 0.01 −0.01 −0.02 −0.02 0.01 −0.03 −0.02 −0.03 0.01
5.58 7.11 −4.25 3.38 8.07 5.85 −1.20 3.09 9.26 8.16 −2.49 4.10
Whole egg total solids (%)
−0.03 0.05 0.12 0.14 −0.07 0.41 0.21 0.27 0.14 0.71 0.19 0.18
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Figure 1. Interaction of housing system × egg storage on shell dynamic stiffness (P < 0.05).
HOUSING SYSTEM AND EGG QUALITY DURING STORAGE
compression shell strength was greatest for enriched cage. The rate of change in egg quality characteristics was not different among the 3 systems at 4, 6, or 12 wk of extended cold storage with the exception of egg weight at 4 wk. When data for all 3 production systems were considered, albumen height, Haugh unit, static compression shell strength, vitelline membrane strength, vitelline membrane deformation, and yolk index all decreased significantly with extended cold storage. The results of the current study show that under commercial management, conventional cage, enriched cage, and aviary housing systems result in eggs of high quality with an equivalent rate of quality decline during storage which should be adequately defined by current USDA grade standards (USDA, 2000).
ACKNOWLEDGMENTS The authors appreciate the laboratory contributions of Patsy Mason and Bradley Covington (USDA, Agricultural Research Service) throughout this project.
REFERENCES Abrahamsson, P., and R. Tauson. 1998. Performance and egg quality of laying hens in an aviary system. J. Appl. Poult. Res. 7:225–232. Anderson, K. E. 2012. Final Report of the Thirty Eighth North Carolina Layer Performance and Management Test. NC Cooperative Extension Service. Vol. 38, No. 5. Accessed Aug. 8, 2013. http://www.ces.ncsu.edu/depts/poulsci/tech_manuals/layer_re ports/38_final_report.pdf. Biladeau, A. M., and K. M. Keener. 2009. The effects of edible coatings on chicken egg quality under refrigerated storage. Poult. Sci. 88:1266–1274. De Ketelaere, B., T. Govaerts, P. Coucke, E. Dewil, J. Visscher, E. Decuypere, and J. De Baerdemaeker. 2002. Measuring the eggshell strength of 6 different genetic strains of laying hens: Techniques and comparisons. Br. Poult. Sci. 43:238–244. De Reu, K., T. B. Rodenburg, K. Grijspeerdt, W. Messens, M. Heyndricks, F. A. M. Tuyttens, B. Sonck, J. Zoons, and L. Herman. 2009. Bacteriological contamination, dirt, and cracks of eggshells in furnished cages and noncage systems for laying hens: An international on-farm comparison. Poult. Sci. 88:2442–2448. Fromm, D., and G. Matrone. 1962. A rapid method for evaluating the strength of the vitelline membrane of the hen’s egg yolk. Poult. Sci. 41:1516–1521. Funk, E. M. 1944. Effects of Temperature and Humidity on the Keeping Quality of Shell Eggs. Missouri Agric. Exp. Sta. Bull. No. 382. University of Missouri, Columbia. Guesdon, V., and J. M. Faure. 2004. Laying performance and egg quality in hens kept in standard or furnished cages. Anim. Res. 53:45–57. Haugh, R. R. 1937. The Haugh unit for measuring egg quality. US Egg Poult. Mag. 43:552–555, 572–573. Hidalgo, A., M. Luciasano, E. M. Comelli, and C. Pompei. 1996. Evolution of chemical and physical yolk characteristics during the storage of shell eggs. J. Agric. Food Chem. 44:1447–1452. Hidalgo, A., M. Rossi, F. Clerici, and S. Ratti. 2008. A market study on the quality characteristics of eggs from different housing systems. Food Chem. 106:1031–1038. Holt, P. S., R. H. Davies, J. Dewulf, R. K. Gast, J. K. Huwe, D. R. Jones, D. Waltman, and K. R. Willian. 2011. The impact of different housing systems on egg safety and quality. Poult. Sci. 90:251–262. Jones, D. R., K. C. Lawrence, S. C. Yoon, and G. W. Heitschmidt. 2010. Modified pressure imaging for egg crack detection and resulting egg quality. Poult. Sci. 89:761–765.
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1-mm probes (compared with a 75-mm disc in the current study), thus assessing the strength of a very small portion of the vitelline membrane and resulting in very low force measurements. During extended cold storage, the elasticity of the vitelline membrane decreased (distance membrane deformed before rupture decreased), which concurs with Jones et al. (2005, 2010). Utilizing a capillary tube assessment method, Fromm and Matrone (1962) found vitelline membrane elasticity to increase with egg age, but the capillary assessment method is much more subjective. Yolk index assessments were not different between housing systems, nor were the rate of change in yolk index different at 4, 6, or 12 wk of storage. Overall, yolk index did decrease with egg age. Fromm and Matrone (1962) reported similar findings and Oosterwoud (1987) and Hidalgo et al. (1996) reported water moves into the yolk during egg storage, which results in a widening and flattening of the yolk. Static compression shell strength was found to be greatest for enriched eggs and significantly lower for aviary. The difference between the average values was 1 N. No clear trend was found in static compression shell strength during storage. At 8 wk, a significant decrease in shell strength was observed, but values had returned to previous levels by 10 wk. Jones and Musgrove (2005) found no significant changes in static compression shell strength during 10 wk of cold storage. Eggs from the 3 housing systems had different responses to shell dynamic stiffness during storage. Mertens et al. (2006) reported aviary eggs to have significantly higher shell dynamic stiffness, with enriched and conventional cage eggs being similar and free range eggs being lowest. The change in shell dynamic stiffness at 4, 6, and 12 wk of extended cold storage was not different among the housing systems, even with enriched eggs consistently experiencing a decline in values as aviary eggs increased in dynamic stiffness. These results substantiate the conclusions of Lin et al. (1996), that the nonhomogeneous and irregular shape of the egg causes accurate strain or stress analysis of the shell by analytical methods to be virtually impossible. Average whole egg total solids were not significantly different between the 3 housing systems. Hidalgo et al. (2008) determined total solids for conventional cage, free range, and barn produced retail eggs were not different. Additionally, whereas whole egg total solids increased slightly during storage (0.30 %), the increased level at 12 wk was not significantly different from 0 wk. Jones et al. (2010) also reported a slight insignificant increase in whole egg total solids during 5 wk of cold storage. The rate of change in whole egg total solids was not different among housing systems at 4, 6, and 12 wk of storage. Overall, differences were found between housing systems for egg weight, albumen height, Haugh unit, and static compression shell strength. Aviary and enriched systems produced slightly heavier eggs (<1 g) than conventional cage. Albumen height and Haugh unit were greater for conventional cage production. Static
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Jones et al. USDA. 2000. United States standards, grades, and weight classes for shell eggs. AMS 56. Accessed August 8, 2013. http://www. ams.usda.gov/AMSv1.0/getfile?dDocName=STELDEV3004376. USDA. 2008. Regulations governing the voluntary grading of shell eggs. 7 CFR part 56. Accessed August 8, 2013. http://www.ams. usda.gov/AMSv1.0/getfile?dDocName=STELDEV3004690. Van Den Brand, H., H. K. Parmentier, and B. Kemp. 2004. Effects of housing system (outdoor vs cages) and age of laying hens on egg characteristics. Br. Poult. Sci. 45:745–752. Varguez-Montero, G., L. Sarmiento-Franco, R. Santos-Ricalde, and J. Segura-Correa. 2012. Egg production and quality under three housing systems in the tropics. Trop. Anim. Health Prod. 44:201–204. Vits, A., D. Weitzenbürger, H. Hamann, and O. Distl. 2005. Production, egg quality, bone strength, claw length, and keel bone deformities of laying hens housed in furnished cages with different group sizes. Poult. Sci. 84:1511–1519. Wall, H. 2011. Production performance and proportion of nest eggs in layer hybrids housed in different designs of furnished cages. Poult. Sci. 90:2153–2161. Wall, H., and R. Tauson. 2002. Egg quality in furnished cages for laying hens—Effects of crack reduction measures and hybrid. Poult. Sci. 81:340–348. Wang, X. L., J. X. Zheng, Z. H. Ning, L. J. Qu, G. Y. Xu, and N. Yang. 2009. Laying performance and egg quality of blueshelled layers as affected by different housing systems. Poult. Sci. 88:1485–1492.
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Jones, D. R., and M. T. Musgrove. 2005. Effects of extended storage on egg quality factors. Poult. Sci. 84:1774–1777. Jones, D. R., M. T. Musgrove, A. B. Caudill, P. A. Curtis, and J. K. Northcutt. 2005. Microbial quality of cool water washed shell eggs. Int. J. Poult. Sci. 4:938–943. Jones, D. R., J. B. Tharrington, P. A. Curtis, K. E. Anderson, K. M. Keener, and F. T. Jones. 2002. Effects of cryogenic cooling of shell eggs on egg quality. Poult. Sci. 81:727–733. Keener, K. M., K. C. McAvoy, J. B. Foegeding, P. A. Curtis, K. E. Anderson, and J. A. Osborne. 2006. Effect of testing temperature on internal egg quality measurements. Poult. Sci. 85:550–555. Lin, J., V. M. Puri, and R. C. Anantheswaran. 1996. Strains in eggshell during cooling of eggs – Measurement and prediction using the finite element method. Trans. ASAE 39:1005–1012. Mertens, K., F. Bamelis, B. Kemps, B. Kamers, E. Verhoelst, B. De Ketelaere, M. Bain, E. Decuypere, and J. De Baerdemaeker. 2006. Monitoring of eggshell breakage and eggshell strength in different production chains of consumption eggs. Poult. Sci. 85:1670–1677. Oosterwoud, A. 1987. Effect of egg handling on egg quality. Poult. Sci. Symp. 20:283–291. SAS Institute. 2002. SAS/STAT User’s Guide. Version 9.3. SAS Institute Inc., Cary, NC. Silversides, F. G., and P. Villeneuve. 1994. Is the Haugh unit correction for egg weight valid for eggs stored at room temperature? Poult. Sci. 73:50–55. Singh, R., K. M. Cheng, and F. G. Silversides. 2009. Production performance and egg quality of four strains of laying hens kept in conventional cages and floor pens. Poult. Sci. 88:256–264.
Key words: sustainable, egg production, housing, egg quality, storage 2014 Poultry Science 93:1282–1288 http://dx.doi.org/10.3382/ps.2013-03631
INTRODUCTION The US egg industry has expanded to offer a variety of purchasing options to consumers. This expansion has occurred due to market demands and legislative actions defining animal confinement parameters. Traditionally, laying hens in the United States have been housed in conventional cages. A great deal is known on the effects of conventional cages on egg production, egg quality, and egg safety. A volume of research has examined the effect of alternative housing systems on egg quality and safety in the European Union (Abrahamsson and Tauson, 1998; Wall and Tauson, 2002; Guesdon
©2014 Poultry Science Association Inc. Received September 18, 2013. Accepted November 29, 2013. 1 Research support provided in part by a grant from the Coalition for a Sustainable Egg Supply (Kansas City, MO). 2 Corresponding author: [email protected]
and Faure, 2004; Van Den Brand et al., 2004; Vits et al., 2005; Hidalgo et al., 2008; De Reu et al., 2009; Wall, 2011). Unfortunately, many of the outcomes cannot be directly transferred to United States alternative housing systems due to substantial differences in hen management, hen genetics, and egg holding methods between the United States and European Union (Holt et al., 2011). Controlled production studies provide a clearer understanding of the effects of housing systems on egg production and quality (Anderson, 2012). Under such conditions, hens in each housing system are provided identical nutrition, controlled lighting, and other management considerations. Commercial hen production studies provide a real world perspective, as hens are managed in an appropriate manner to maximize economic impact. Commercial studies relinquish scientific control of hen management, yet provide invaluable information on commercial application of housing systems.
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ABSTRACT Egg producers in the United States are utilizing a variety of commercial egg production systems to provide consumer choice and meet legislative requirements. Consumer egg grades in the United States were developed for conventional cage production, and it is unclear what effect alternative production systems might have on egg quality during retail and consumer home storage. The current study was undertaken to determine what changes in egg quality characteristics occur during extended cold storage for commercially produced conventional cage, enriched colony cage, and cage-free aviary eggs. During 12 wk of cold storage, egg weight, albumen height, Haugh unit, static compression shell strength, vitelline membrane strength and deformation, yolk index, shell dynamic stiffness, and whole egg total solids were monitored. Overall, aviary and enriched eggs were significantly (P < 0.05) heavier than conventional cage. Albumen height and Haugh unit (P
HOUSING SYSTEM AND EGG QUALITY DURING STORAGE
MATERIALS AND METHODS Pullets The experimental protocol was approved by the Michigan State University Institutional Animal Care and Use Committee. Lohmann White laying hens were housed at a commercial egg facility located in the Midwest United States. The pullets were housed in conventional cages or cage-free aviary (aviary) rearing systems. Pullets in the conventional cages were provided 247.74 cm2 (38.4 in2) with 15 birds per cage. Pullets had access to 4.06 cm (1.6 in) of feeder space per bird with 7.5 birds per nipple water. The aviary rearing system had 218 birds per cage with 159.94 cm2 (24.79 in2) of cage space, 2.18 cm (0.86 in) of perch space, and 4.37 cm (1.72 in) of feeder space per bird with 11 birds per nipple water from 0 to 9 wk of age. From 9 to 18 wk, the pullets had additional cage space provided, increasing the total cage space available by 248.97 cm2 (38.59 in2) and 1.09 cm (0.43 in) of perch space. Seven additional nipple waters resulted in 8 birds per nipple. The pullets also had floor access from 6 to 18 wk, providing 100.13 cm2 (15.52 in2) per bird. The pullets were housed at 19 wk of age in 3 different housing systems (conventional cage, aviary, and enriched colony cage) and depopulated at 77 wk of age.
Housing Systems Conventional Cage. The conventional cage house was a belted, preexisting commercial house with a hen population of 193,424. The conventional house consisted of 10 rows of conventional cages with 8 tiers and a walkway between tiers 4 and 5. The conventional cage provided 567.75 cm2 (88 in2) per bird with 6 birds per
cage. Each conventional cage provided 10.16 cm (4 in) of feeder space per bird and 6 hens per nipple water. The house was tunnel ventilated and had manure removed every 3 to 4 d. Enriched Colony Cage. The enriched colony house was a belted, newly built facility housing 46,795 laying hens. The facility consisted of 5 rows of colony cages with 4 tiers per row. Each enriched colony cage contained 60 birds that provided 753.22 cm2 (116.75 in2) of physical space. Each colony cage provided several amenities (expressed on a per bird basis), including 12.07 cm (4.75 in) of feeder space, 17.73 cm (6.98 in) of perch space, 63.03 cm2 (9.77 in2) of nest space, 26.52 cm2 (4.11 in2) of scratch pad space, and 7.5 birds per water line nipple with drip cup. The house had ceiling inlets and was cross-ventilated with manure removal every 3 to 4 d. Cage-Free Aviary. The cage-free aviary system (aviary) was ventilated the same as the enriched colony system and was a newly built facility housing 49,842 laying hens. The aviary had 6 rows of housing, with litter access on the bird side and a human aisle on the opposite side. The row length was divided by wire partitions that created 10 compartments of laying hens. The population size consisted of 852 laying hens per compartment along the 2 exterior sides of the facility and 1,704 laying hens per compartment in the 2 interior rows. This provided each hen in the exterior compartments with 1,170.71 cm2 (181.46 in2) and interior compartments with 1,166.45 cm2 (180.80 in2) of total area. The area was calculated within the aviary system as 547.03 cm2 (84.79 in2) of cage wire space and 103.61 cm2 (16.06 in2) of solid surface plates; for exterior compartment floor access, 319.35 cm2 (49.50 in2) under the aviary and 200.71 cm2 (31.11 in2) in front of the aviary; and for interior compartment floor access, 319.35 cm2 (49.50 in2) under the aviary and 196.39 cm2 (30.44 in2) in front of the aviary. Irrespective of compartment location, hens had access to 10.19 cm (4.01 in) of feeder space, 15.24 cm (6 in) of perch space [11.86 cm (4.67 in) inside the housing system and 3.38 cm (1.33 in) in the forage area], 86.32 cm2 (13.38 in2) of nest space area, and 8.9 birds per nipple water.
Lighting and Diet The 3 housing systems were located on a single farm and experienced identical seasonal temperature fluctuations. The photoperiod at time of lay was 16L:8D with a light intensity of 10 lx. Laying hens had ad libitum access to water and were fed commercially available diets formulated to maximize production efficiency. The cage-free aviary feeding schedule consisted of 5 feedings a day for 16 min each. The enriched colony and conventional cage had 2 feedings a day for 16 min each, with the scratch augers in the enriched colony running at the same time as a feeding for 30 s.
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Egg quality declines as an egg ages (Silversides and Villeneuve, 1994; Jones et al., 2002, 2010; Jones and Musgrove, 2005; Biladeau and Keener, 2009). Defined quality parameters exist for eggs marketed in the United States (USDA, 2000) specifying egg grades. Each state in the United States has a defined period of time eggs can be marketed in retail, usually 30 or 45 d postprocessing. During this time, eggs must maintain the quality grade standards (USDA, 2000) identified on the carton (generally grade A). Egg processing guidelines (USDA, 2008) and quality standards in the United States are based on conventional cage egg production. It is unknown if current US egg guidelines and standards are appropriate for ensuring the quality and safety of eggs produced from commercial alternative production systems. The current study was undertaken to determine the effect of commercial conventional cage, enriched colony cage, and cage-free aviary (aviary) egg production on various egg quality factors during extended cold storage.
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Egg Processing and Storage
Egg Quality Assessments Each sample time, 12 to 18 eggs per treatment were screened via candling to remove cracked eggs before egg quality assessments were conducted. The number of eggs examined for each treatment was dependent on the total number of intact eggs received per treatment during egg replicate shipment. Eggs were removed from cold storage immediately before egg quality assessments were conducted to ensure comparable egg temperatures. Egg temperature was monitored throughout quality assessments and ranged between 7 to 9°C. Egg quality measurements were tracked for individual eggs with the exception of whole egg solids, which were conducted on pools. Each egg was assessed 3 times for shell dynamic stiffness on an acoustical egg tester (KU Leuven, Leuven, Belgium) as described by De Ketelaere et al. (2002). Individual egg weights were recorded with a TSS QCD system (Technical Services and Supplies, Dunnington, York, United Kingdom). Shell static compression strength was measured with a texture analyzer (TA-XT2plus; Texture Technologies, Scarsdale, NY) equipped with a 5-kg load cell and 3-in. diameter aluminum compressions disc (TA-30, Texture Technologies). The egg was presented on its side in an egg holder with posts (TA-650, Texture Technologies). A test speed of 2 mm/s and a trigger force of 0.001 kg were used. Albumen height and Haugh unit (Haugh, 1937) were recorded with the TSS QCD system. Yolk index was determined by measuring yolk height with a tripod micrometer (S-6428; B.C. Ames Inc., Melrose, MA) and yolk width with a digital micrometer (Thermo Fisher Scientific, Waltham, MA). The yolk was separated from albumen before vitelline membrane strength and deformation were measured with a texture analyzer (TA-XT2plus; Texture Technologies) according to the procedures of Jones et al. (2010). The albumen and
Statistical Analysis Data collected during the study were subjected to an ANOVA utilizing the PROC GLM analysis in SAS (SAS Institute, 2002). Housing system and week of storage were the main effects. The decline in egg quality during storage was determined for each parameter monitored in the study at 4 (28 d), 6 (42 d), and 12 wk (84 d) and compared between housing systems. The time points for egg quality decline analysis were selected based on individual US state allowances for eggs to be marketed (generally 30 or 45 d) and also to account for in-home consumer storage. The average change in each egg quality measurement for a housing system between 0 wk and the set sample times was calculated for each egg storage set replicate. The rate of quality decline was then analyzed using the ANOVA as implemented within PROC GLM to determine if housing system differences existed.
RESULTS AND DISCUSSION The average values for all monitored egg quality indicators throughout the 12 wk of cold storage are presented in Table 1. Eggs from the aviary and enriched systems were heavier than those from conventional cages (58.69 and 58.88 vs. 57.97 g; P < 0.05). Though the difference was significant, less than a gram of difference in average egg weight was found between the systems. Albumen height and Haugh unit were greater (5.81 mm and 74.61, respectively; P < 0.05) for conventional cage eggs compared with those from the enriched system. Static compression shell strength was greater (P < 0.05) for enriched system eggs (39.57 N) than aviary (38.53 N). No significant differences were observed between housing treatments for average values of vitelline membrane strength, vitelline membrane deformation (elasticity), yolk index, shell dynamic stiffness, or whole egg percent total solids. The combined egg quality values for all treatments during each week of storage are presented in Table 2. Overall, egg weight did not significantly change during 12 wk of cold storage. Albumen height and Haugh unit decreased (P < 0.05) throughout storage, with the highest values (7.21 mm and 84.62, respectively) occurring at 0 wk and lowest values (4.80 mm and 66.21, respectively) measured at 12 wk. A lower (P < 0.05) static compression shell strength was found at 8 wk of storage compared with all other monitoring times. Vitelline membrane strength and deformation decreased throughout storage (P < 0.05), with the greatest levels (1.77 N and 7.84 mm, respectively) detected at 0 wk and lowest levels (1.17 N and 6.17 mm, respectively)
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Eggs were collected from each housing system on 4 occasions (hen age 26, 41, 57, and 70 wk) and shipped to the laboratory overnight. Immediately upon arrival, eggs were washed with a pilot egg washer under recommended USDA guidelines (USDA, 2008) according to the procedures described by Jones et al. (2005). The pilot egg washer had been modified to contain 60 eggs per wash cycle and commercial egg wash detergent was used (Exalt II; Zee Company Inc., Chattanooga, TN). After washing and drying procedures were complete, eggs were placed in clean foam cartons (Dolco Packaging, Decatur, IN) and stored at 4°C for the remainder of the study. Eggs were allowed to equilibrate to the refrigerated temperature overnight before conducting 0 wk assessments due to egg temperature effects on egg quality measurements (Keener et al., 2006). Subsequent egg testing was conducted every other week through 12 wk of storage.
yolk from 3 eggs were combined to form 4 to 6 pools per treatment (dependent on replicate). Whole egg total solids were determined according to the procedures of Jones et al. (2010). Triplicate measurements were made per pool.
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HOUSING SYSTEM AND EGG QUALITY DURING STORAGE Table 1. Effect of housing system on average values for egg quality indicators throughout 12 wk of cold storage
Housing system
Egg weight (g)
Albumen height (mm)
Aviary Conventional cage Enriched colony cage SE
58.69a 57.97b 58.88a 0.25
5.68b 5.81a 5.57b 0.05
a,bMeans
Haugh unit
Shell strength (N)
Vitelline membrane strength (N)
Vitelline membrane deformation (mm)
73.58ab 74.61a 72.60b 0.43
38.53b 39.36ab 39.57a 0.30
1.45 1.40 1.40 0.03
7.00 6.85 6.81 0.06
Yolk index
Shell dynamic stiffness1 (kN/m)
Whole egg total solids1 (%)
0.47 0.48 0.47 0.01
158.68 159.93 159.95 0.58
23.23 23.13 23.20 0.03
within a column with different letters are significantly different (P < 0.05). housing system × egg storage interaction (P < 0.05).
1Significant
2 g heavier than at 0 wk, whereas aviary and enriched eggs weighed less than 0 wk eggs from those systems (−0.27 and −1.88 g, respectively). The differences in change in egg weight between housing systems during the first 4 wk of storage could be due to variability within housing systems on the size of eggs being produced. Additionally, eggs were randomly selected for each monitoring period and conventional cage eggs at 4 wk of storage during the fourth replicate of the study were heavier than the 0-wk eggs. Otherwise, no differences were noted in the rate of decline for any egg quality parameters measured between the housing systems at 4, 6, and 12 wk of storage. In the current study, egg weights were significantly greater for aviary and enriched cages compared with conventional cage production. This differs from Guesdon and Faure (2004), who reported no difference in egg weights between conventional and enriched cages. Jones et al. (2010) found egg weight during 5 wk of cold storage to be highly variable, which agrees with the current study when considering the rate of egg weight changes during storage for the 3 housing systems. Additionally, in the current study, no differences were observed in average egg weights compared between storage weeks when all housing systems were combined. Jones and Musgrove (2005) also reported fairly consistent egg weights during 10 wk of cold storage. Albumen height and Haugh unit values decreased during storage in the current study, which concurs with the findings of others (Jones et al., 2002, 2005, 2010; Biladeau and Keener, 2009). Overall, albumen height and
Table 2. Effect of extended cold storage on egg quality indicators
Item Egg storage (wk) 0 2 4 6 8 10 12 SE a–fMeans
Egg weight (g)
Albumen height (mm)
58.41 58.22 58.47 58.64 58.60 58.57 58.68 0.38
7.21a 6.21b 5.64c 5.64c 5.17d 5.13d 4.80e 0.07
Haugh unit
Shell strength (N)
Vitelline membrane strength (N)
Vitelline membrane deformation (mm)
84.62a 78.24b 73.69c 73.72c 69.54d 69.16d 66.21e 0.68
39.47a 39.18a 39.21a 40.12a 37.58b 39.51a 39.02a 0.46
1.77a 1.52b 1.50bc 1.39cd 1.32de 1.25ef 1.17f 0.04
7.84a 7.11b 7.15b 6.84c 6.56d 6.54d 6.17e 0.10
within a column with different letters are significantly different (P < 0.05). housing system × egg storage interaction (P < 0.05).
1Significant
Yolk index
Shell dynamic stiffness1 (kN/m)
Whole egg total solids1 (%)
0.49a 0.48b 0.48b 0.47bc 0.47bc 0.47bc 0.46c 0.01
157.31 159.34 160.39 160.44 158.80 159.10 161.25 0.91
23.00 23.15 23.05 23.18 23.17 23.39 23.38 0.05
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found at 12 wk. Average yolk index decreased (P < 0.05) throughout storage, ranging from 0.49 to 0.46. A significant housing system × egg storage interaction was found for shell dynamic stiffness (Figure 1) and whole egg total solids (Figure 2). Figure 1 illustrates how eggs from each housing system had different shell dynamic stiffness properties throughout storage. Conventional cage-produced eggs had an increase in shell dynamic stiffness between 0 and 2 wk, which remained fairly constant throughout the remaining sampling periods. Eggs from aviary production had a general increase in shell dynamic stiffness throughout the storage period. Conversely, eggs from enriched production had a general decrease in shell dynamic stiffness throughout the 12 wk of storage. Whole egg total solids generally increased for each housing system through the 12-wk storage period (Figure 2), but the rate of increase was variable for the 3 housing systems, resulting in a housing system × egg storage interaction (P < 0.05). The rate of change at 4, 6, and 12 wk (28, 42, and 84 d) of cold storage, compared with 0 wk values, for each of the monitored egg quality characteristics is presented in Table 3. Comparisons in the rate of change in egg quality were conducted at these points to discern if housing system affected the ability of eggs in retail to meet USDA grade standards for common use by or sale by dates (30 or 45 d postprocessing) and also after storing in consumer refrigerators for an extended period (12 wk). The only occurrence of significance between housing systems was for the change in egg weight at 4 wk, when conventional cage eggs were approximately
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Figure 2. Interaction of housing system × egg storage on whole egg total solids (P < 0.05).
Haugh unit were greater for conventional cage- than enriched cage-produced eggs. Singh et al. (2009) reported greater albumen heights in conventional cage eggs compared with floor hens. Vits et al. (2005) found significant differences between enriched housing systems for Haugh unit scores. Conversely, Wang et al. (2009) found no difference in the average albumen height and Haugh unit values from conventional cage and outdoor production systems. Additionally, Varguez-Montero et al. (2012) found no differences in albumen height and Haugh unit when comparing conventional cage, outdoor, and indoor production systems and Hidalgo et al. (2008) found similar Haugh unit values in Italian retail eggs from free range, cage, and barn production. Whereas the overall albumen height and Haugh unit values were found to be different between conventional and enriched colony cage production in the current study, the rate of decline at 4, 6, and 12 wk of storage
for the 2 parameters was never significantly different between any of the housing systems. No differences were found in overall vitelline membrane strength or elasticity between the housing systems. Previously, vitelline membrane characteristics had not been extensively compared between hen housing systems. When all eggs monitored during the study were considered, vitelline membrane strength and elasticity significantly decreased during extended cold storage. Previous research also found vitelline membrane strength to decrease with increased egg age (Funk, 1944; Fromm and Matrone, 1962; Oosterwoud, 1987; Jones et al., 2002, 2010). Conversely, Jones et al. (2005) and Biladeau and Keener (2009) found no difference in vitelline membrane strength during prolonged storage. In both cases, vitelline membrane strength measurements were assessed via static compression (as was the case in the current study), utilizing approximately
Table 3. Effect of housing system on changes in egg quality factors at 4, 6, and 12 wk of cold storage compared with initial values Egg weight (g)
Housing system 4 wk Aviary Conventional cage Enriched colony cage SE 6 wk Aviary Conventional cage Enriched colony cage SE 12 wk Aviary Conventional cage Enriched colony cage SE a,bMeans
−0.27b 2.09a −1.88b 0.70 −0.04 2.11 −1.47 0.91 −0.74 1.42 −1.22 0.76
Albumen height (mm)
−1.57 −1.62 −1.60 0.38 −1.35 −1.46 −1.89 0.27 −2.23 −2.48 −2.43 0.41
Haugh unit
−11.21 −11.49 −11.16 3.05 −9.75 −10.21 −13.06 1.79 −16.44 −20.24 −18.74 3.77
Vitelline membrane strength (N)
Shell strength (N)
−0.81 1.06 −0.58 1.53 0.54 0.68 0.50 1.81 −1.09 1.38 −1.43 1.70
−0.26 −0.12 −0.34 0.09 −0.42 −0.20 −0.43 0.12 −0.64 −0.40 −0.61 0.15
Vitelline membrane deformation (mm)
−0.64 −0.27 −0.96 0.28 −1.25 −0.53 −1.10 0.22 −1.87 −1.20 −1.80 0.37
in a column, within an egg age period, with different letters are significantly different (P < 0.05).
Shell dynamic stiffness (kN/m)
Yolk index
−0.01 −0.01 −0.02 0.01 −0.01 −0.02 −0.02 0.01 −0.03 −0.02 −0.03 0.01
5.58 7.11 −4.25 3.38 8.07 5.85 −1.20 3.09 9.26 8.16 −2.49 4.10
Whole egg total solids (%)
−0.03 0.05 0.12 0.14 −0.07 0.41 0.21 0.27 0.14 0.71 0.19 0.18
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Figure 1. Interaction of housing system × egg storage on shell dynamic stiffness (P < 0.05).
HOUSING SYSTEM AND EGG QUALITY DURING STORAGE
compression shell strength was greatest for enriched cage. The rate of change in egg quality characteristics was not different among the 3 systems at 4, 6, or 12 wk of extended cold storage with the exception of egg weight at 4 wk. When data for all 3 production systems were considered, albumen height, Haugh unit, static compression shell strength, vitelline membrane strength, vitelline membrane deformation, and yolk index all decreased significantly with extended cold storage. The results of the current study show that under commercial management, conventional cage, enriched cage, and aviary housing systems result in eggs of high quality with an equivalent rate of quality decline during storage which should be adequately defined by current USDA grade standards (USDA, 2000).
ACKNOWLEDGMENTS The authors appreciate the laboratory contributions of Patsy Mason and Bradley Covington (USDA, Agricultural Research Service) throughout this project.
REFERENCES Abrahamsson, P., and R. Tauson. 1998. Performance and egg quality of laying hens in an aviary system. J. Appl. Poult. Res. 7:225–232. Anderson, K. E. 2012. Final Report of the Thirty Eighth North Carolina Layer Performance and Management Test. NC Cooperative Extension Service. Vol. 38, No. 5. Accessed Aug. 8, 2013. http://www.ces.ncsu.edu/depts/poulsci/tech_manuals/layer_re ports/38_final_report.pdf. Biladeau, A. M., and K. M. Keener. 2009. The effects of edible coatings on chicken egg quality under refrigerated storage. Poult. Sci. 88:1266–1274. De Ketelaere, B., T. Govaerts, P. Coucke, E. Dewil, J. Visscher, E. Decuypere, and J. De Baerdemaeker. 2002. Measuring the eggshell strength of 6 different genetic strains of laying hens: Techniques and comparisons. Br. Poult. Sci. 43:238–244. De Reu, K., T. B. Rodenburg, K. Grijspeerdt, W. Messens, M. Heyndricks, F. A. M. Tuyttens, B. Sonck, J. Zoons, and L. Herman. 2009. Bacteriological contamination, dirt, and cracks of eggshells in furnished cages and noncage systems for laying hens: An international on-farm comparison. Poult. Sci. 88:2442–2448. Fromm, D., and G. Matrone. 1962. A rapid method for evaluating the strength of the vitelline membrane of the hen’s egg yolk. Poult. Sci. 41:1516–1521. Funk, E. M. 1944. Effects of Temperature and Humidity on the Keeping Quality of Shell Eggs. Missouri Agric. Exp. Sta. Bull. No. 382. University of Missouri, Columbia. Guesdon, V., and J. M. Faure. 2004. Laying performance and egg quality in hens kept in standard or furnished cages. Anim. Res. 53:45–57. Haugh, R. R. 1937. The Haugh unit for measuring egg quality. US Egg Poult. Mag. 43:552–555, 572–573. Hidalgo, A., M. Luciasano, E. M. Comelli, and C. Pompei. 1996. Evolution of chemical and physical yolk characteristics during the storage of shell eggs. J. Agric. Food Chem. 44:1447–1452. Hidalgo, A., M. Rossi, F. Clerici, and S. Ratti. 2008. A market study on the quality characteristics of eggs from different housing systems. Food Chem. 106:1031–1038. Holt, P. S., R. H. Davies, J. Dewulf, R. K. Gast, J. K. Huwe, D. R. Jones, D. Waltman, and K. R. Willian. 2011. The impact of different housing systems on egg safety and quality. Poult. Sci. 90:251–262. Jones, D. R., K. C. Lawrence, S. C. Yoon, and G. W. Heitschmidt. 2010. Modified pressure imaging for egg crack detection and resulting egg quality. Poult. Sci. 89:761–765.
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1-mm probes (compared with a 75-mm disc in the current study), thus assessing the strength of a very small portion of the vitelline membrane and resulting in very low force measurements. During extended cold storage, the elasticity of the vitelline membrane decreased (distance membrane deformed before rupture decreased), which concurs with Jones et al. (2005, 2010). Utilizing a capillary tube assessment method, Fromm and Matrone (1962) found vitelline membrane elasticity to increase with egg age, but the capillary assessment method is much more subjective. Yolk index assessments were not different between housing systems, nor were the rate of change in yolk index different at 4, 6, or 12 wk of storage. Overall, yolk index did decrease with egg age. Fromm and Matrone (1962) reported similar findings and Oosterwoud (1987) and Hidalgo et al. (1996) reported water moves into the yolk during egg storage, which results in a widening and flattening of the yolk. Static compression shell strength was found to be greatest for enriched eggs and significantly lower for aviary. The difference between the average values was 1 N. No clear trend was found in static compression shell strength during storage. At 8 wk, a significant decrease in shell strength was observed, but values had returned to previous levels by 10 wk. Jones and Musgrove (2005) found no significant changes in static compression shell strength during 10 wk of cold storage. Eggs from the 3 housing systems had different responses to shell dynamic stiffness during storage. Mertens et al. (2006) reported aviary eggs to have significantly higher shell dynamic stiffness, with enriched and conventional cage eggs being similar and free range eggs being lowest. The change in shell dynamic stiffness at 4, 6, and 12 wk of extended cold storage was not different among the housing systems, even with enriched eggs consistently experiencing a decline in values as aviary eggs increased in dynamic stiffness. These results substantiate the conclusions of Lin et al. (1996), that the nonhomogeneous and irregular shape of the egg causes accurate strain or stress analysis of the shell by analytical methods to be virtually impossible. Average whole egg total solids were not significantly different between the 3 housing systems. Hidalgo et al. (2008) determined total solids for conventional cage, free range, and barn produced retail eggs were not different. Additionally, whereas whole egg total solids increased slightly during storage (0.30 %), the increased level at 12 wk was not significantly different from 0 wk. Jones et al. (2010) also reported a slight insignificant increase in whole egg total solids during 5 wk of cold storage. The rate of change in whole egg total solids was not different among housing systems at 4, 6, and 12 wk of storage. Overall, differences were found between housing systems for egg weight, albumen height, Haugh unit, and static compression shell strength. Aviary and enriched systems produced slightly heavier eggs (<1 g) than conventional cage. Albumen height and Haugh unit were greater for conventional cage production. Static
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Jones et al. USDA. 2000. United States standards, grades, and weight classes for shell eggs. AMS 56. Accessed August 8, 2013. http://www. ams.usda.gov/AMSv1.0/getfile?dDocName=STELDEV3004376. USDA. 2008. Regulations governing the voluntary grading of shell eggs. 7 CFR part 56. Accessed August 8, 2013. http://www.ams. usda.gov/AMSv1.0/getfile?dDocName=STELDEV3004690. Van Den Brand, H., H. K. Parmentier, and B. Kemp. 2004. Effects of housing system (outdoor vs cages) and age of laying hens on egg characteristics. Br. Poult. Sci. 45:745–752. Varguez-Montero, G., L. Sarmiento-Franco, R. Santos-Ricalde, and J. Segura-Correa. 2012. Egg production and quality under three housing systems in the tropics. Trop. Anim. Health Prod. 44:201–204. Vits, A., D. Weitzenbürger, H. Hamann, and O. Distl. 2005. Production, egg quality, bone strength, claw length, and keel bone deformities of laying hens housed in furnished cages with different group sizes. Poult. Sci. 84:1511–1519. Wall, H. 2011. Production performance and proportion of nest eggs in layer hybrids housed in different designs of furnished cages. Poult. Sci. 90:2153–2161. Wall, H., and R. Tauson. 2002. Egg quality in furnished cages for laying hens—Effects of crack reduction measures and hybrid. Poult. Sci. 81:340–348. Wang, X. L., J. X. Zheng, Z. H. Ning, L. J. Qu, G. Y. Xu, and N. Yang. 2009. Laying performance and egg quality of blueshelled layers as affected by different housing systems. Poult. Sci. 88:1485–1492.
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Jones, D. R., and M. T. Musgrove. 2005. Effects of extended storage on egg quality factors. Poult. Sci. 84:1774–1777. Jones, D. R., M. T. Musgrove, A. B. Caudill, P. A. Curtis, and J. K. Northcutt. 2005. Microbial quality of cool water washed shell eggs. Int. J. Poult. Sci. 4:938–943. Jones, D. R., J. B. Tharrington, P. A. Curtis, K. E. Anderson, K. M. Keener, and F. T. Jones. 2002. Effects of cryogenic cooling of shell eggs on egg quality. Poult. Sci. 81:727–733. Keener, K. M., K. C. McAvoy, J. B. Foegeding, P. A. Curtis, K. E. Anderson, and J. A. Osborne. 2006. Effect of testing temperature on internal egg quality measurements. Poult. Sci. 85:550–555. Lin, J., V. M. Puri, and R. C. Anantheswaran. 1996. Strains in eggshell during cooling of eggs – Measurement and prediction using the finite element method. Trans. ASAE 39:1005–1012. Mertens, K., F. Bamelis, B. Kemps, B. Kamers, E. Verhoelst, B. De Ketelaere, M. Bain, E. Decuypere, and J. De Baerdemaeker. 2006. Monitoring of eggshell breakage and eggshell strength in different production chains of consumption eggs. Poult. Sci. 85:1670–1677. Oosterwoud, A. 1987. Effect of egg handling on egg quality. Poult. Sci. Symp. 20:283–291. SAS Institute. 2002. SAS/STAT User’s Guide. Version 9.3. SAS Institute Inc., Cary, NC. Silversides, F. G., and P. Villeneuve. 1994. Is the Haugh unit correction for egg weight valid for eggs stored at room temperature? Poult. Sci. 73:50–55. Singh, R., K. M. Cheng, and F. G. Silversides. 2009. Production performance and egg quality of four strains of laying hens kept in conventional cages and floor pens. Poult. Sci. 88:256–264.