The word "quality" means many things. The definitions include: an essential or distinctive characteristic, property, or attribute; character with respect to fineness or grade of excellence; and high grade, superiority, excellence. All of these definitions can easily be applied to eggs, and consumers have different expectations of "quality" for eggs.

In general, egg quality can be broken out into three criteria: microbial, physical, and functional. Microbial quality relates to the presence of general microorganisms. These organisms could be indicators of general cleanliness, those that cause product spoilage, or foodborne pathogens. Eggs are a raw agricultural commodity and are perishable (i.e., they require refrigeration to reduce the likelihood of spoilage, decay, and growth of pathogenic organisms). Safe handling and cooking instructions are required for eggs according to 21 CFR 101.17(h).¹ The primary pathogenic organism of concern for eggs and egg products is Salmonella spp., with particular emphasis placed on Salmonella Enteritidis.

The physical quality of eggs is generally defined by U.S. Department of Agriculture (USDA) Agricultural Marketing Service (AMS) voluntary standards.² U.S. egg physical quality is broken out into shell, air cell, albumen (white), and yolk characteristics. Consumers have expectations of clean, unbroken shells with a normal shape. When candled or cracked open, consumers accept a relatively small air cell present in the large end of the egg. The albumen should be clear and free of inclusions (blood spots, meat spots, other particulates), with limited amount of thin albumen and a thick albumen that is tall and easily visible. The yolk is expected to be an acceptable shade of deep yellow to deep orange, depending on the regional preference for yolk color. The yolk should remain intact during cracking and cooking (fried, over-easy, poaching, etc.) and be slightly off-center when cracked on a flat surface.

Eggs provide many functional characteristics³ to food formulations. From aeration of baked goods and confections to emulsification for sauces, dressings, and batters, eggs are a food formulation wonder. When consumers and food manufacturers include eggs in a food matrix, multiple functional properties are often enhanced due to the complex of proteins, lipids, and other components naturally found in eggs.

Many factors can influence the microbial, physical, and functional qualities of eggs. It is often difficult to pinpoint an exact root cause of an egg quality issue due to the complexity of egg production, processing, distribution, and end-user handling. To take a more systematic approach, the authors discuss factors associated with egg quality through each phase from production to the end user.

Laying Hen Production and Management

The U.S. and many other countries are shifting from intensive to more extensive housing systems for laying hens. The shift in housing and management strategies has resulted in changes in egg microbial and physical egg quality. In 2011, a group of international collaborators published a review of the impacts of hen housing systems on egg safety and quality.⁴ A key takeaway from this review was that it is difficult to compare research outcomes regarding the impacts of hen housing on egg safety and quality due to the dramatic differences in extensive housing systems found around the world. Extensive housing systems vary greatly in design, construction, hen movement, egg collection, and the number of hens in a housing segment, among other factors. All of these factors can influence the microbial flora present in the environment, as well as the predominant microbial populations within the laying hen.

A group of researchers partnered with a commercial egg products producer to conduct an examination of the impacts of conventional cage, enriched colony, and cage-free aviary housing on affordability, environmental impact, worker health, animal wellbeing, and food safety.⁵ Regarding food safety, it was determined that components of hen housing systems⁶ impacted the levels to total aerobes and Enterobacteriaceae present in the production environment, as well as Salmonella and Campylobacter spp. detection. Aviary drag swabs and enriched colony nest pads were found to be highly contaminated with Enterobacteriaceae and Campylobacter spp. The detection of pathogens on the shells of eggs was not different among the three housing systems. The authors indicate that nest box usage in extensive housing systems is important to enhance the microbial quality of eggs produced. Eggs laid outside the nest box in extensive housing systems have been identified as having a greater food safety risk in several studies.^6,7,8

Regardless of housing system, the quicker eggs are refrigerated, the more egg microbial and physical quality are retained. Salmonella Enteritidis and many other pathogenic organisms do not grow well at 45 °F (7.2 °C). Salmonella Enteritidis can sometimes be found in either the yolk or albumen of eggs laid by infected hens, usually in very small numbers of bacterial cells when the eggs are freshly laid.⁹ Albumen is a harsh environment for these bacteria, but yolk contains abundant nutrients that can support rapid and extensive microbial growth. At warm temperatures, Salmonella Enteritidis can multiply to reach much larger levels in yolk and even migrate into the yolk from the albumen. Prompt refrigeration of eggs acts to slow or halt both the migration and growth of Salmonella Enteritidis in eggs so that any contaminants are less likely to pose a high risk of illness for consumers.¹⁰ Physical qualities of the egg also degrade at a lower rate during refrigerated storage.

Two U.S. programs oversee egg safety at the farm: the U.S. Food and Drug Administration (FDA) Egg Rule and the USDA Animal and Plant Health Inspection Service (APHIS) National Poultry Improvement Plan. The FDA Egg Rule¹¹ has many requirements, one of which is that eggs must be refrigerated in an ambient temperature of 45 °F (7.2 °C) or lower within 36 hours of lay. The Egg Rule is written specifically to control for Salmonella Enteritidis. Additional Egg Rule requirements include:

• Hens must come from Salmonella Enteritidis-negative flocks
• Environmental testing must be performed for Salmonella Enteritidis at prescribed points in the lifecycle of the flock
• A pest management plan must be in place
• A written Salmonella Enteritidis prevention plan, unique for each production farm, is required
• A biosecurity plan is required.

FDA or trained FDA representatives visit farms for inspection and publish the findings.

Salmonella Enteritidis deposition inside eggs can lead to transmission from infected laying hens to their chicks, so provisions of the National Poultry Improvement Plan (NPIP) are targeted to reduce the presence of this pathogen in breeding flocks and hatcheries.¹² Certification as Salmonella Enteritidis-clean under NPIP standards requires hatcheries and breeder facilities to be regularly cleaned and disinfected; documentation that hatcheries and chicks entering multiplier breeder flocks originate from Salmonella Enteritidis-clean grandparent flocks; use of feed that has been produced, treated, and handled to minimize contamination risks; effective insect and rodent control; testing of hatchery debris and the laying house environment to detect Salmonella Enteritidis contamination; and blood testing of hens to detect infection.

Shell Egg Processing

In the U.S., eggs enter a shell egg processing facility in one of two ways. Inline processing involves a series of belts that move the eggs directly from the production barns to the processing equipment. Under this scenario, eggs are generally processed for the end user within 24 hours of being laid. Depending on how the facility chooses to operate, eggs from individual barns may be separated; most often, however, eggs from multiple barns blend on the belt entering the processing facility. This can present challenges during a traceback.

In offline processing, eggs are gathered at the farm and transported multiple times each week to the shell egg processing facility. To meet Egg Rule requirements, offline (nest run) eggs must be transported under refrigeration to the processing facility and remain under refrigeration until the time of processing. Due to the potential of thermal cracks occurring when exposing cold eggs to warm processing conditions, nest run eggs are allowed to temper at room temperature in the processing room for up to 36 hours before processing. While offline eggs are generally older than inline eggs at the time of processing, it is often easier to segregate individual barns/farms as lots of eggs during processing, which is helpful during a traceback.

Enhancing the safety and quality of processed shell eggs starts with clean equipment. Effective sanitation programs¹³ in processing facilities reduce the likelihood of microbial contamination of eggs being introduced by the processing equipment. Previous research^14,15 has shown that shell egg processing facility sanitation was not effective at the time. Since the completion of these studies, new emphasis has been placed on facility sanitation programs. Pre-operational sanitation inspection is also a component of the USDA-AMS voluntary shell egg grading program. AMS has partnered with USDA's Agricultural Research Service (ARS) and Purdue University to produce a series of training videos¹⁶ (in both English and Spanish) to explain expectations of AMS egg processing facility sanitation.

Shell egg processing requirements vary depending on where a processing facility is located, where eggs are being sold, and whether the facility participates in the AMS Voluntary Grading of Shell Eggs.¹⁷ The commercial egg washing practices utilized in the U.S. generally follow the conditions prescribed by AMS including:

• Eggs must be spray washed
• Wash water must be at least 90 °F (32.2 °C) or 20 °F (11 °C) warmer than the warmest egg
• Wash water must contain an approved detergent
• Eggs must receive a warm water sanitizing rinse or the equivalent
• Eggs must be blown dry before packaging.

Eggs not processed under the voluntary AMS program must follow individual state egg laws.¹⁸

Washing eggs at warm temperatures causes egg temperature to increase.¹⁹ Egg packaging material²⁰ also influences the rate of egg cooling post-processing. The rapid cooling of eggs has been examined^21,22 to assist with dropping egg temperature to the desired 45 °F (7 °C) or lower as soon as possible after processing to retain microbial and physical quality.

After eggs are processed for end users, eggs must be maintained in an ambient temperature no greater than 45 °F (7 °C), according to USDA's Food Safety and Inspection Service (FSIS), including transportation.²³ FDA has a requirement for the same maximum egg storage temperature at retail.²⁴ Research²⁵ has shown that fewer than 24 hours at room temperature has a greater impact on yolk quality decline than 15 weeks in refrigeration. Furthermore, regardless of whether eggs were washed or not, under refrigerated storage, egg quality was similar.

Eggs and the End User

Eggs are regulated through receipt by the end user to ensure egg safety and product quality. What happens when the end user takes possession? The egg producer's name, contact information, and processing information for the eggs are on the packaging. When a product quality or food safety concern arises, rarely is the end user questioned.

Eggs are a highly nutritious food and are available worldwide. There are many cultural differences as to how eggs should be produced and handled. In the age of digital information and social media, consumers are quick to share "information." Unfortunately, as far as eggs are concerned, the information shared by consumers is not always accurate. It is important to ensure that the proper handling, storage, and use of eggs is communicated to a broad audience in manners that are relatable.

References

1. Code of Federal Regulations. Title 21, Chapter I, Subchapter B, Part 101, Subpart A § 101.17. "Food labeling warning, notice, and safe handling statements: Shell eggs." https://www.ecfr.gov/current/title-21/chapter-I/subchapter-B/part-101/subpart-A/section-101.17#p-101.17(h)(1).
2. U.S. Department of Agriculture Agricultural Marketing Service (USDA-AMS). United States Standards, Grades, and Weight Classes for Shell Eggs: AMS 56." July 20, 2000. https://www.ams.usda.gov/sites/default/files/media/Shell_Egg_Standard%5B1%5D.pdf.
3. American Egg Board. "20+ Functional Benefits of Eggs." 2023. http://incredibleegg.wpenginepowered.com/wp-content/uploads/2023/06/AEB_20plus_FunctionalitySheet_2023.pdf.
4. Holt, P. S., R. H. Davies, J. Dewulf, et al. "The impact of different housing systems on egg safety and quality." Poultry Science 90, no. 1 (January 2011): 251–262. https://www.sciencedirect.com/science/article/pii/S0032579119320851.
5. Coalition for Sustainable Egg Supply. "Final Research Results Report." https://www2.sustainableeggcoalition.org/document_center/download/public/CSESResearchResultsReport.pdf.
6. Jones, D. R., N. A. Cox, J. Guard, et al. "Microbiological impact of three commercial laying hen housing systems." Poultry Science 94, no. 3 (March 2015): 544–551. https://www.sciencedirect.com/science/article/pii/S0032579119386031.
7. De Reu, K., K. Grijspeerdt, M. Heyndrickx, et al. "Bacterial shell contamination in the egg collection chains of different housing systems for laying hens." British Poultry Science 47, no. 2 (2006). https://www.tandfonline.com/doi/full/10.1080/00071660600610773.
8. Jones, D. R. and K. E. Anderson. "Housing system and laying hen strain impacts on egg microbiology." Poultry Science 92, no. 8 (August 2013): 2221–2225. https://www.sciencedirect.com/science/article/pii/S0032579119388285.
9. Gantois, Inne, Richard Ducatelle, Frank Pasmans, et al. "Mechanisms of egg contamination by Salmonella Enteriditis." FEMS Microbiology Reviews 33, no. 4 (July 2009): 718–738. https://academic.oup.com/femsre/article/33/4/718/583518?login=true.
10. Gast, Richard K., Dana K. Dittoe, and Steven C. Ricke. "Salmonella in eggs and egg-laying chickens: Pathways to effective control." Critical Reviews in Microbiology (December 30, 2022). https://www.tandfonline.com/doi/full/10.1080/1040841X.2022.2156772.
11. Code of Federal Regulations. Title 21, Chapter I, Subchapter B, Part 118. "Production, Storage, and Transportation of Shell Eggs." July 9, 2009. https://www.ecfr.gov/current/title-21/chapter-I/subchapter-B/part-118.
12. USDA Animal and Plant Health Inspection Service (APHIS). "National Poultry Improvement Plan (NPIP)." Last updated June 2, 2020. https://www.aphis.usda.gov/aphis/ourfocus/animalhealth/nvap/nvap-reference-guide/poultry/national-poultry-improvement-plan.
13. Alvarado, Christine and Deana Jones. "Egg Production: Clean from the Start = Success at the Finish!" Food Safety Magazine. February 26, 2021. https://www.food-safety.com/articles/6992-egg-production-clean-from-the-start-success-at-the-finish.
14. Jones, D. R., J. K. Northcutt, M. T. Musgrove, et al. "Survey of Shell Egg Processing Plant Sanitation Programs: Effects on Egg Contact Surfaces." Journal of Food Protection 66, no. 8 (August 2003): 1486–1489. https://www.sciencedirect.com/science/article/pii/S0362028X2203229X.
15. Musgrove, M. T., D. R. Jones, J. K. Northcutt, et al. "Survey of Shell Egg Processing Plant Sanitation Programs: Effects on Non-Egg-Contact Surfaces." Journal of Food Protection 67, no. 12 (December 2004): 2801–2804. https://www.sciencedirect.com/science/article/pii/S0362028X2203784X.
16. Purdue Extension. "Egg Processing & Production Videos: Egg Sanitation." YouTube. https://www.youtube.com/playlist?list=PLtXSf1tu3Jd-FMRe0wIQYnOyAFpTakk-I.
17. Code of Federal Regulations. Title 7, Subtitle B, Chapter I, Subchapter C, Part 56. "Voluntary Grading of Shell Eggs." https://www.ecfr.gov/current/title-7/subtitle-B/chapter-I/subchapter-C/part-56.
18. National Egg Regulatory Officials. "Egg State Laws & Regulations." 2023. https://nerous.org/state-laws-regulations.php.
19. Koelkebeck, K. W., P. H. Patterson, K. E. Anderson, et al. "Temperature Sequence of Eggs from Oviposition through Distribution: Processing—Part 2." Poultry Science 87, no. 6 (June 2008): 1187–1194. https://www.sciencedirect.com/science/article/pii/S0032579119393198.
20. Czarick, Michael and Stan Savage. "Egg Cooling Characteristics in Commercial Egg Coolers." Journal of Applied Poultry Research 1, no. 2 (July 1992): 258–270. https://www.sciencedirect.com/science/article/pii/S1056617119319361.
21. Jones, D. R., J. B. Tharrington, P. A. Curtis, et al. "Effects of cryogenic cooling of shell eggs on egg quality." Poultry Science 81, no. 5 (May 2002): 727–733. https://www.sciencedirect.com/science/article/pii/S0032579119436456.
22. Thompson, J. F., J. Knutson, R. A. Ernst, et al. "Rapid Cooling of Shell Eggs." Journal of Applied Poultry Research 9, no. 2 (July 2000): 258–268. https://www.sciencedirect.com/science/article/pii/S1056617119309511.
23. Code of Federal Regulations. Title 9, Chapter III, Subchapter I, Part 590, Subpart A. "Subpart A—General." https://www.ecfr.gov/current/title-9/chapter-III/subchapter-I/part-590/subpart-A.
24. Code of Federal Regulations. Title 21, Chapter I, Subchapter B, Part 115. "Shell Eggs." https://www.ecfr.gov/current/title-21/chapter-I/subchapter-B/part-115.
25. Jones, D. R., G. E. Ward, P. Regmi, and D. M. Karcher. "Impact of egg handling and conditions during extended storage on egg quality." Poultry Science 97, no. 2 (February 2018): 716–723. https://www.sciencedirect.com/science/article/pii/S0032579119309265.

Deana Jones is a Research Food Technologist at the U.S. National Poultry Research Center in Athens, Georgia, which is part of the U.S. Department of Agriculture's Agricultural Research Service (USDA-ARS).

Richard Gast is a Supervisory Microbiologist at the U.S. Poultry Research Center's Egg and Poultry Production Safety Research Unit in Athens, Georgia, which is part of USDA-ARS.