doi: 10.15389/agrobiology.2019.4.667eng

UDC: 636.5:636.082:591.3



Yu.I. Zabudskii

Russian State Agrarian Correspondence University, 1, ul. Fuchika, Balashikha, Moscow Province, 143900 Russia, e-mail

Zabudskii Yu.I.

Received May 14, 2019


Storage of eggs causes the death of the blastoderm cells, including necrosis and apoptosis (S. Bloom et al., 1998). Depending on the storage conditions (duration, temperature, and air humidity), the physicochemical parameters of egg ingredients vary. Water and CO2 move through the shell, leading to an increase in pH of the albumen and yolk, which changes the activity of enzymes, reduces bactericidal properties of albumen and yolk. Violation of amino acid composition and ratio is characteristic of the yolk, and lipid peroxidation is developing (M.N. Argunov et al., 2015). Destruction and increased permeability of the vitelline membrane and the internal eggshell membranes occur. The secondary sexual ratio shifts (M. McDonald, 1960; M. Tagirov, 2010; M. Boerjan, 2016). The efficiency of egg incubation decreases as well as chick yield (G. Fasenko, 1992; V. Christensen et al., 2001; K. Tona et al., 2003; P. Hristakieva, 2011; D. Terčič et al., 2016). Immunocompetence of chickens hatched from stored eggs lowers (M. Goliomytis et al., 2015). These hatchlings need elevated temperature of environment during the first weeks of life (S. Yalcin et al., 2014). Haugh units, albumen and yolk indexes, albumen pH, etc., being indicators of the stored egg quality (P. Tsarenko, 2015), vary depending on genotype, age and feeding, the stress of the parents, and the season. Each next day of storage following 2 days post egg laying needs an additional one-hour incubation period for compensation. The degree of embryo development in the freshly laid eggs is not the same in different bird species. The stage of embryogenesis depends on age, mother’s type of use (for eggs, for meat, or for dual use), and the order of the egg in the cycle of egg laying. Eggs with embryos which reach the gastrula stage are less sensitive to storage (I. Reijrink et al., 2008). Reduced hatching can be partially leveled by different methods, including heating during storage which provides development to the specified stage of embryogenesis (I. Kosin, 1956; M. Petek et al, 2004; Y. Piestun et al, 2013; D. Nicholson et al., 2013; L. Dyadichkina et al., 2016). Their positive effect is limited by the egg quality, modes of storage and heating (temperature, frequency and duration of exposure), as well as incubation.

Keywords: poultry, egg hatching, storage, ontogenesis, quality assessment methods, preventive methods.



  1. Fasenko G.M. Egg storage and the embryo. Poultry Science, 2007, 86(5): 1020-1024 CrossRef
  2. Tona K., Malheiros R.D., Bamelis F., Careghi C., Bruggeman V., Moraes V.M., Onagbesan O., Decuypere E. Effects of storage time on incubating egg gas pressure, thyroid hormones and corticosterone levels in embryos, and their hatching parameters. Poultry Science, 2003, 82(5): 840-845 CrossRef
  3. Tsarenko P.P. Ptitsevodstvo, 2010, 4: 45-47 (in Russ.).  
  4. Eyal-Giladi H., Kochav S. From cleavage to primitive streak formation: a complementary normal table and a new look at the first stages of development of the chick. I. General morphology. Developmental Biology, 1976, 49(2): 321-337 CrossRef
  5. Bakst M.R., Gupta S.K., Akuffo V. Comparative development of the turkey and chicken embryo from cleavage through hypoblast formation. Poultry Science, 1997, 76(1): 83-90 CrossRef
  6. Sellier N., Brillard J.-P., Dupuy V., Bakst M.R. Comparative staging of embryo development in chicken, turkey, duck, goose, guinea fowl, and Japanese quail assessed from five hours after fertilization through seventy-two hours of incubation. Journal of Applied Poultry Research, 2006, 15(2): 219-228 CrossRef
  7. Arora K.L., Kosin I.L. Changes in the gross morphological appearance of chicken and turkey blastoderms during preincubation storage. Poultry Science, 1966, 45(4): 819-825 CrossRef
  8. Bakst M.R., Akuffo V., Nicholson D., French N. Comparison of blastoderm traits from 2 lines of broilers before and after egg storage and incubation. Poultry Science, 2012, 91(10): 2645-2648 CrossRef
  9. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. Journal of Morphology, 1951, 88(1): 49-92 CrossRef
  10. Meijerhof R. Pre-incubation holding of hatching eggs. World's Poultry Science Journal, 1992, 48(1): 57-68 CrossRef
  11. Pokhrel N., Ben-Tal Cohen E., Genin O., Sela-Donenfeld D., Cinnamon Y. Cellular and morphological characterization of blastoderms from freshly laid broiler eggs. Poultry Science, 2017, 96(12): 4399-4408 CrossRef
  12. Fasenko G.M., Hardin R.T., Robinson F.E., Wilson J.L. Relationship of hen age and egg sequence position with fertility, hatchability, viability, and preincubation embryonic development in broiler breeders. Poultry Science, 1992, 71(8): 1374-1383 CrossRef
  13. Steinke L. Keimscheibeuntersuchungen an hühnereiern unter besonderer berücksichtigung des entwicklungszustandes. Archiv für Geflügelkunde, 1972, 36(1): 5-10.
  14. Reijrink I.A.M., Meijerhof R., Kemp B., van Den Brand H. The chicken embryo and its micro environment during egg storage and early incubation. World's Poultry Science Journal, 2008, 64(4): 581-598 CrossRef
  15. Fasenko G.M., Robinson F.E., Whelan A.I., Kremeniuk K.M., Walker J.A. Prestorage incubation of long-term stored broiler breeder eggs. 1. Effects on hatchability. Poultry Science, 2001, 80(10): 1406-1411 CrossRef     
  16. Bolotnikov A.M., Shurakov A.I., Kamenskii Yu.N., Dobrinskii L.N. Ekologiya rannego ontogeneza ptits [Ecology of early ontogenesis in birds]. Sverdlovsk, 1985 (in Russ.).  
  17. Fasenko G.M., Robinson F.E., Hardin R.T. Research note: variability in preincubation embryonic development in domestic fowl. 2. Effect of duration of egg storage period. Poultry Science, 1992, 71(12): 2129-2132 CrossRef
  18. Fasenko G.M., Wilson J.L., Robinson F.E., Hardin R.T. Effects of length of egg nest holding time and high environmental temperatures on pre-storage embryonic development, survival, and hatchability of broiler breeders. Journal of Applied Poultry Research, 1999, 8(4): 488-492 CrossRef
  19. Bakst M.R., Akuffo V. Impact of egg storage on embryonic development. Avian and Poultry Biology Reviews, 2002, 13(7): 125-131 CrossRef
  20. Bloom S.E., Muscarella D.E., Lee M.Y., Rachlinski M. Cell death in the avian blastoderm: resistance to stress-induced apoptosis and expression of anti-apoptotic genes. Cell Death and Differentiation, 1998, 5(6): 529-538 CrossRef
  21. Hamidu J.A., Uddin Z., Li M., Fasenko G.M., Guan L.L., Barreda D.R. Broiler egg storage induces cell death and influences embryo quality. Poultry Science, 2011, 90(8): 1749-1757 CrossRef
  22. Dyadichkina L.F., Pozdnyakova N.S., Melekhina T.A., Goldin Yu.S., Yukhacheva N.A., Minakhina V.A. Ptitsa i ptitseprodukty, 2017, 2: 60-62 (in Russ.).  
  23. Hristakieva P., Lalev M., Oblakova M., Mincheva N., Ivanova I. Effect of storage duration on the quality of hatching turkey eggs. Archiva Zootechnica, 2011, 14(3): 57-65.
  24. Tsarenko P.P., Kuleshova L.A. Izvestiya Sankt-Peterburgskogo gosudarstvennogo agrarnogo universiteta, 2015, 40: 112-117 (in Russ.).  
  25. Tsarenko P.P., Vasil'eva L.T. Ptitsevodstvo, 2016, 11: 29-34 (in Russ.).  
  26. Belitz H.-D., Grosch W., Schieberle P. Eggs. In: Food chemistry. Springer, Berlin, Heidelberg, 2009: 546-562 CrossRef
  27. Baron F., Nau F., Guerin-Dubiard C., Bonnassie S., Gautier M., Andrews S.C., Jan S. Egg white versus Salmonella Enteritidis! A harsh medium meets a resilient pathogen. Food Microbiology, 2016, 53(B): 82-93 CrossRef
  28. Mori M., Masuda N. Proteins of the vitelline membrane of quail (Coturnix coturnix japonica) eggs. Poultry Science, 1993, 72(8): 1566-1572 CrossRef
  29. Brake J., Walsh T.J., Benton C.E., Jr., Petitte J.N., Meijerhof R., Penalva G. Egg handling and storage. Poultry Science, 1997, 76(1): 144-151 CrossRef
  30. Chen J., Thesmar S.H., Kerr W.L. Outgrowth of Salmonellae and the physical property of albumen and vitelline membrane as influenced by egg storage conditions. Journal of Food Protection, 2005, 68(12): 2553-2558 CrossRef
  31. Demirel Ş., Kırıkçi K. Effect of different egg storage times on some egg quality characteristics and hatchability of pheasants (Phasianus colchicus). Poultry Science, 2009, 88(2): 440-444 CrossRef
  32. Samli H.E., Agma A., Senkoylu N. Effects of storage time and temperature on egg quality in old laying hens. Journal of Applied Poultry Research, 2005, 14(3): 548-553 CrossRef
  33. Christensen V. Factors associated with early embryonic mortality. Worlds Poultry Science Journal, 2001, 57(4): 359-372 CrossRef
  34. Argunov M.N., Stepanov V.A., Petunina K.V. Vestnik Voronezhskogo gosudarstvennogo agrarnogo universiteta, 2015, 4(47/2): 66-75 (in Russ.).  
  35. Mather C.M., Laughlin K.F.  Storage of hatching eggs: The effect on early embryonic development. British Poultry Science, 1977, 18(5): 597-603 CrossRef
  36. Yalcin S., Gursel I., Bilgen G., Izzetoglu G.T., Horuluoglu B.H., Gucluer G. Egg storage duration and hatch window affect gene expression of nutrient transporters and intestine morphological parameters of early hatched broiler chicks. Animal, 2015, 1: 1-7 CrossRef
  37. Tona K., Bamelis F., De Ketelaere B., Bruggeman V., Moraes V.M.B., Buyse J., Onagbesan O., Decuypere E. Effects of egg storage time on spread of hatch, chick quality, and chick juvenile growth. Poultry Science, 2003, 82(5): 736-774 CrossRef
  38. Petek M., Baspinar H., Ogan M., Balci F. Effects of egg weight and length of storage period on hatchability and subsequent laying performance of quail. Turkish Journal of Veterinary and Animal Sciences, 2005, 29(2): 537-542.
  39. Terčič D., Pestotnik M. Effects of flock age, prestorage heating of eggs, egg position during storage and storage duration on hatchability parameters in layer parent stock. Acta argiculturae Slovenica, 2016, 5: 138-142.
  40. Stern C.D. The sub-embryonic fluid of the egg of the domestic fowl and its relationship to the early development of the embryo.In: Avian incubation. S.G. Tullett (ed.). Butterworth-Heinemann, London, 1991: 81-90.
  41. McDonald M.W. Effect of temperature of storage and age of fowl eggs on hatchability and sex ratio, growth, and viability of the chickens. Australian Journal of Agricultural Research, 1960, 11(4): 664-672 CrossRef
  42. Tagirov M.T.Biotechnologia, 2010, 3(3): 84-91 (in Russ.).  
  43. Boerjan M. Pre-storage incubation and SPIDES: New procedures in hatching egg storage. Pas Reform, 2014. Available Accessed 24.07.2019.
  44. Silversides F.G., Scott T.A. Effect of storage and layer age on quality of eggs from two lines of hens. Poultry Science, 2001, 80(8): 1240-1245 CrossRef
  45. Bagliacca M., Paci G., Marzoni M. Effect of egg weight categories, storage time and storage temperature on incubation length in duck eggs (Cairina moschata L. and Anas platyrhynhos domestica L.). The Journal of Poultry Science, 2005, 42(3): 205-214 CrossRef
  46. Romao J.M., Moraes T.G.V., Teixeira R.S.C., Cardoso W.M., Buxade C.C. Effect of egg storage length on hatchability and weight loss in incubation of egg and meat type Japanese quails. Brazilian Journal of Poultry Science, 2008, 10(3): 143-147 CrossRef
  47. Christensen V.L., Wineland M.J., Fasenko G.M., Donaldson W.E. Egg storage effects on plasma glucose and supply and demand tissue glycogen concentrations of broiler embryos. Poultry Science, 2001, 80(12): 1729-1735 CrossRef
  48. Jones D.R., Curtis P.A., Anderson K.E., Jones F.T. Microbial contamination in inoculated shell eggs: II. Effects of layer strain and egg storage. Poultry Science, 2004, 83(1): 95-100 CrossRef
  49. Lapão C., Gama L.T., Chaveiro Soares M. Effects of broiler breeder age and length of egg storage on albumen characteristics and hatchability. Poultry Science, 1999, 78(5): 640-645 CrossRef
  50. Tona K., Onagbesan O., De Ketelaere D., Decuypere E., Bruggeman V. Effects of age of broiler breeders and egg storage on egg quality, hatchability, chick quality, chick weight, and chick posthatch growth to forty-two days. Journal of Applied Poultry Research, 2004, 13(1): 10-18 CrossRef
  51. Shim M.Y., Pesti G.M., Bakalli R.I., Edwards H.M. Jr. The effect of breeder age and egg storage time on phosphorus utilization by broiler progeny fed a phosphorus deficiency diet with 1-OH vitamin D3. Poultry Science, 2008, 87(6): 1138-1145 CrossRef
  52. Yalcin S., Bilgen G., Gursel I. Effect of egg storage duration on brooding temperature requirements of broilers. Proc. XIVth European Poultry Conference. Stavanger, Norway, June 23-27, 2014. Stavanger, 2014: 608.
  53. Tona K., Bamelis F., De Ketelaere B., Bruggeman V., Decuypere E. Effect of induced molting on albumen quality, hatchability, and chick body weight from broiler breeders. Poultry Science, 2002, 81(3): 327-332 CrossRef
  54. KrivopishinI.P. Ozon v promyshlennom ptitsevodstve [Ozone in industrial poultry farming]. Moscow, 1988 (in Russ.).  
  55. Reijrink I.A.M., van Duijvendijk L.A.G., Meijerhof R., Kemp B., van den Brand H.  Influence of air composition during egg storage on egg characteristics, embryonic development, hatchability, and chick quality. Poultry Science, 2010, 89(9): 1992-2000 CrossRef
  56. Elibol O., Brake J. Effect of egg position during three and fourteen days of storage and turning frequency during subsequent incubation on hatchability of broiler hatching eggs. Poultry Science, 2008, 87(6): 1237-1241 CrossRef
  57. Popova L.A., Komarchev A.S. Ptitsevodstvo, 2014, 2: 10-13 (in Russ.).  
  58.  Akpinar G., Canogullari S., Baylan M., Alasahan S., Aygun A. The use of propolis extract for the storage of quail eggs. Journal Applied Poultry Research, 2015, 24(4): 427-435 CrossRef
  59. Kosin I.L. Studies on pre-incubation warming of chicken and turkey eggs. Poultry Science, 1956, 35(6): 1384-1392 CrossRef
  60. Coleman J.W., Siegel P.B. Selection for body weight at eight weeks of age: 5. Embryonic stage at oviposition and its relationship to hatchability. Poultry Science, 1966, 45(5): 1008-1011 CrossRef
  61. Fasenko G.M., Christensen V.L., Wineland M.J., Petitte J.N. Examining the effects of prestorage incubation of turkey breeder eggs on embryonic development and hatchability of eggs stored for four or fourteen days. Poultry Science, 2001, 80(2): 132-138 CrossRef
  62. Petek M., Dikmen S. The effects of pre-storage incubation of quail breeder eggs on hatchability and subsequent growth performance of progeny. Animal Research, 2004, 53(6): 527-534 CrossRef
  63. Gucbilmez M., Ozlu S., Shiranjang R., Elibol O., Brake J. Effects of pre-incubation heating of broiler hatching eggs during storage, flock age, and length of storage period on hatchability. Poultry Science, 2013, 92(12): 3310-3313 CrossRef
  64. Piestun Y., Druyan S., Brake J., Yahav S. Thermal treatments prior to and during the beginning of incubation affect phenotypic characteristics of broiler chickens post hatching. Poultry Science, 2013, 92(4): 882-889 CrossRef
  65. Silva F.H.A., De Faria D.E., Torres K.A.A., De Faria Filho D.E., Coelho A.A.D., Savino V.J.M. Influence of egg pre-storage heating period and storage length on the digestive tract of newly-hatched broiler chicks. Brazilian Journal of Poultry Science, 2008, 10(1): 17-22 CrossRef
  66. Kgwatalala P.M., Faki O., Nsoso S.J. Influence of pre-storage incubation on the hatchability of guinea fowl eggs stored for fourteen days. Journal of Animal Science Advances, 2013, 3(6): 304-309 CrossRef
  67. Reijrink I.A.M., Meijerhof R., Kemp B., Graat E.A.M., van Den Brand H. Influence of pre storage incubation on embryonic development, hatchability, and chick quality. Poultry Science, 2009, 88(12): 2649-2660 CrossRef
  68. Dymond J., Vinyard B., Nicholson A.D., French N.A., Bakst M.R. Short periods of incubation during egg storage increase hatchability and chick quality in long-stored broiler eggs. Poultry Science, 2013, 92(11): 2977-2987 CrossRef
  69. Dyadichkina L.F., Pozdnyakova N.S., Melekhina T.A., Goldin Yu.S., Kolomeitsev V.A., Minakhina V.A., Yukhacheva N.A. Ptitsevodstvo, 2016, 9: 2-6 (in Russ.).  
  70. Decuypere E., Michels H. Incubation temperature as a management tool: a review. World’s Poultry Science Journal, 1992, 48(1): 28-38 CrossRef
  71. Zabudskii Yu.I., Kiselev L.Yu., Delyan A.S., Kamalov R.A., Golikova A.P., Fedoseeva N.A., Myshkina M.S. Problemy biologii produktivnykh zhivotnykh, 2012, 1: 5-16 (in Russ.).
  72. Rukovodstvo po inkubatsii Hubbard Balt Iza, 2013. Available No date.
  73. Fisinin V.I., Dyadichkina L.F., Goldin Yu.S. et al. Tekhnologiya inkubatsii yaits sel'skokhozyaistvennoi ptitsy: metodicheskie nastavleniya [The technology of poultry eggs incubation: instructions]. Sergiev Posad, 2011 (in Russ.).
  74. Sarkisyan S., Abramyan V., Mkhchyan E. Ptitsevodstvo, 2009, 4: 39-40 (in Russ.).  
  75. Gast R.K., Holt P.S. Influence of the level and location of contamination on the multiplication of Salmonella enteritidis at different storage temperatures in experimentally inoculated eggs. Poultry Science, 2000, 79(4): 559-563 CrossRef
  76. Bakst M.R., Welch G.R., Camp M.J. Observations of turkey eggs stored up to 27 days and incubated for 8 days: embryo developmental stage and weight differences and the differentiation of fertilized from unfertilized germinal discs. Poultry Science, 2016, 95 (5): 1165-1172 CrossRef
  77. Mailyan E. Agrorynok, 2009, 5: 16-18 (in Russ.).
  78. Grikhina N.V., Galkina Yu.Yu. Materialy Mezhdunarodnoi nauchno-prakticheskoi konferentsii «Problemy i perspektivy razvitiya nauki i obrazovaniya» (Kishinev, 06 iyunya 2017 goda) [Proc. Int. Conf. «Problems and prospects for the development of science and education» (Kishinev, June 06, 2017)]. Kishinev, 2017: 62-66 (in Russ.).
  79. Haque M.A., Pearson J.T., Hou P.-D.L., Tazawa H. Effects of pre-incubating egg storage on embryonic functions and growth. Respiration Physiology, 1996, 103(1): 89-98 CrossRef
  80. Zabudskii Yu.I. Reproductive function in hybrid poultry. III. An impact of breeder flock age (review). Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2015, 50(4): 444-457 CrossRef
  81. Goliomytis M., Tsipouzian T., Hager-Theodorides A.L. Effects of egg storage on hatchability, chick quality, performance and immunocompetence parameters of broiler chickens. Poultry Science, 2015, 94(9): 2257-2265 CrossRef
  82. Chen C., Sander J.E., Dale N.M. The effect of dietary lysine deficiency on the immune response to Newcastle disease vaccination in chickens. Avian Diseases, 2003, 47(4): 1346-1351 CrossRef
  83. Damaziak K., Pawęska M., Gozdowski D., Niemiec J. Short periods of incubation, egg turning during storage and broiler breeder hens age for early development of embryos, hatching results, chicks quality and juvenile growth. Poultry Science, 2018, 97(9): 3264-3276 CrossRef
  84. Rocha J.S.R., Baiao N.C., Barbosa V.M., Pompeu M.A., Fernabdes M.N.S., Lara L.J.C., Matias C.F.O., Batista J.V.M.S.P. Negative effects of fertile storage on the egg and the embryo and suggested hatchery management to minimize such problems. World’s Poultry Science Journal, 2013, 69(1): 35-44 CrossRef
  85. Özlü S., Elibol O., Brake J. Effect of storage temperature fluctuation on embryonic development and mortality, and hatchability of broiler hatching eggs. Poultry Science, 2018, 97(11): 3878-3883 CrossRef
  86. Jones D.R.D., Karcher M., Regmi P., Robison C.O., Gast R.K. Hen genetic strain and extended cold storage influence on physical egg quality from cage-free aviary housing system. Poultry Science, 2018, 97(7): 2347-2355 CrossRef
  87. Yılmaz A., Tepeli C., Garip M., Cağlayan T. The effects of incubation temperature on the sex of Japanese quail chicks. Poultry Science, 2011, 90(10): 2402-2406 CrossRef
  88. Nicholson D., French N., Tullett  S., van Lierde E., Jun G. Short periods of incubation during egg storage — SPIDES. Lohmann Information, 2013, 48(2): 51-61.
  89. Zabudskii Yu.I. Povyshenie adaptatsii broilerov k intensivnoi tekhnologii otkorma posredstvom okhlazhdeniya inkubiruemykh yaits s progressivno uvelichivayushcheisya ekspozitsiei. Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 1993, 28(4): 69-74 (in Russ.).
  90. Zabudskii Yu.I., Shuvalova M.V. Materialy XVII Mezhdunaronoi konferentsii Vsemirnoi nauchnoi assotsiatsii po ptitsevodstvu (15-17 maya 2012 goda, Sergiev Posad) [Proc. XVII Int. Conf. of the World's Poultry Science Association (May 15-17, 2012, Sergiev Posad)]. Sergiev Posad, 2012: 240-242 (in Russ.).
  91. Zabudskii Yu.I., Golikova A.P., Fedoseeva N.A. Heat training for prenatal period of ontogenesis as a method to increase the thermotolerance in poultry (review). Sel'skokhozyaistvennaya biologiya [Agricultural Biology], 2012, 47(4): 14-21 CrossRef (in Russ.).
  92. Artemov A.D. Problemy biologii produktivnykh zhivotnykh, 2014, 1: 5-20 (in Russ.).
  93. Zhuchkova N.A. Vestnik Orlovskogo GAU, 2017, 1(64): 81-85 CrossRef (in Russ.).
  94. Hamidu J.A., Torres C.A., Johnson-Dahl M.L., Korver D.R. Physiological response of broiler embryos to different incubator temperature profiles and maternal flock age during incubation. 1. Embryonic metabolism and day-old chick quality. Poultry Science, 2018, 97 (8): 2934-2946 CrossRef







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