A meta-analysis of the effect of gamma irradiation on chicken meat quality: Microbiology and colour Meta-analysis of the effect of gamma irradiation in chicken meat
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Abstract
A meta-analysis of the effect of gamma irradiation on the microbial status and colour in raw chicken meat was performed. A total of 14 studies were selected and data about the total viable count (TVC), coliforms (TCC), instrumental colour measurements - lightness (L*), redness (a*) and yellowness (b*) was extracted for evaluation in gamma treated and untreated meat. Due to the high between study heterogeneity, the meta-analysis was conducted through random-effects model applied on the raw mean difference (effect size) for each outcome of interest. The results of the meta-analysis showed that gamma irradiation considerably decreased TVC and TCC (P<0.001). Gamma rays also significantly diminished L* (P=0.013), but increased a* and b* (P<0.001). The meta-regression models showed that the dose of the radiation contributed to the overall effect of irradiation TVC (P=0.006), TCC (P=0.074) and a*(P=0.007). The effect of gamma rays on TVC was further influenced by storage (P=0.007), while package affected the increase of a* (P=0.100).
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References
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Arshad, M. S., Amjad, Z., Yasin, M., Saeed, F., Imran, A., Sohaib, M., Anjum, F. M., Hussain, S. Quality and stability evaluation of chicken meat treated with gamma irradiation and turmeric powder. International Journal of Food Properties, 2019, 22 (1): 154-172. https://doi.org/10.1080/10942912.2019.1575395.
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Bhoir, S. A., Jhaveri, M., Chawla, S. P. (2019). Evaluation and predictive modeling of the effect of chitosan and gamma irradiation on quality of stored chilled chicken meat. Journal of Food Process Engineering, 2019, 42(7): e13254.https://doi.org/10.1111/jfpe.13254.
Borenstein, M., Hedges, L. V., Higgins, J. P. T., Rothstein, H. R. Introduction to meta-analysis. Chichester, UK: John Wiley & Sons, Ltd., 2009.
Borenstein, M., Hedges, L. V., Higgins, J. P. T., Rothstein, H. R. A basic introduction to fixed-effect and random-effects models in meta-analysis. Research Synthesis Methods, 2010, 1: 97-111.https://doi.org/10.1002/jrsm.12.
Brewer, S. (2004). Irradiation effects on meat color – a review. Meat Science, 2004, 68(1): 1–17. https://10.1016/j.meatsci.2004.02
Carriquiry, M., Weber, W. J.,Crooker, B. A. Administration of bovine somatotropin in early lactation: A meta-analysis of production responses by multiparous Holstein cows. Journal of Dairy Science, 2008, 91, 2641–2652.https://doi.org/10.3168/jds.2007-0841.
Chouliara, E., Badeka, A., Savvaidis, I., Kontominas, M. G. Combined effect of irradiation and modified atmosphere packaging on shelf-life extension of chicken breast meat: microbiological, chemical and sensory changes. European Food Research and Technology, 2007, 226(4), 877–888.https://doi.org/10.1007/s00217-007-0610-3.
Correa, W., Brandenburg, J., Behrends, J., Heinbockel, L., Reiling, N., Paulowski, L., Schwudke, D., Stephan,K., Martinez-de-Tejada, G., Brandenburg, K., Gutsmann, T. Inactivation of bacteria by γ-irradiation to investigate the interaction with antimicrobial peptides, Biophysical Journal, 2019, 117 (10): 1805-1819. https://doi.org/10.1016/j.bpj.2019.10.012.
DeCoster, J. Meta-Analysis Notes, 2009. Retrieved on 12.03.2022 from http://www.stat-help.com/notes.html.
Dourou, D., Spyrelli, E. D., Doulgeraki, A. I., Argyri, A. A., Grounta, A., Nychas, G. E., Chorianopoulos, N. G., Tassou, C. C. Microbiota of chicken breast and thigh fillets stored under different refrigeration temperatures assessed by next-generation sequencing. Foods (Basel, Switzerland), 2021,10(4): 765. https://doi.org/10.3390/foods10040765.
Erkmen, O., Bozoglu, T.F. Food Preservation by low temperatures. Food Microbiology: Principles into Practice, 2016, 34–43. https://doi.org/10.1002/9781119237860.ch29.
Fernandez-Duque, E. Comparing and combining data across studies: alternatives to significance testing. Oikos, 1997, 79(3):616.https://doi.org/10.2307/3546906.
Furuta, M., Dohmaru, T., Katayama, T., Toratani, H., Takeda, A. Detection of irradiated frozen meat and poultry using carbon monoxide gas as a probe. Journal of Agricultural and Food Chemistry,1992, 40(7): 1099–1100.https://doi.org/10.1021/jf00019a001.
Gonçalves-Tenório, A., Silva, B. N., Rodrigues, V., Cadavez, V., Gonzales-Barron, U. Prevalence of Pathogens in Poultry Meat: A Meta-Analysis of European Published Surveys. Foods (Basel, Switzerland), 2018, 7(5): 69. https://doi.org/10.3390/foods7050069
Higgins, J. P. T., Thompson, S. G. Quantifying heterogeneity in meta-analysis. Statistics in Medicine, 2002, 21: 1539–1558.https://doi.org/10.1002/sim.1186.
Islam, A., Sadakuzzaman, M., Hossain, M. A., Hossain, M. M., Hashem, M. A. Effect of gamma irradiation on shelf life and quality of indigenous chicken meat: Irradiation on chicken meat. Journal of the Bangladesh Agricultural University, 2019, 17(4): 560–566. https://doi.org/10.3329/jbau.v17i4.44626.
Javanmard, M., Rokni, N., Bokaie, S., Shahhosseini, G. Effects of gamma irradiation and frozen storage on microbial, chemical and sensory quality of chicken meat in Iran. Food Control, 2006, 17(6): 469-473.https://doi.org/10.1016/j.foodcont.2005.02.008.
Kanatt, S. R., Chawla, S. P., Sharma, A. (2015). Effect of radiation processing on meat tenderization. Radiation Physics and Chemistry, 2015,111:1–8. https://doi.org/10.1016/j.radphyschem.2015.02.004
Khalid, W., Arshad, M. S., Yasin, M., Imran, A., Ahmad, M. H. Quality characteristics of gamma irradiation and kale eaf powder treated ostrich and chicken meat during storage. International Journal of Food Properties, 2021, 24:1, 1335-1348. https://doi.org/10.1080/10942912.2021.1963274.
Kralik, G.,Kralik, Z., Grčević, M., Hanžek, D. Quality of chicken meat. In: Animal Husbandry and Nutrition (B. Yücel, T. Taşkin, Eds). IntechOpen, London, 2017. https://doi.org/10.5772/intechopen.72865.
Lacroix, M. Irradiation of foods. In: Emerging Technologies for Food Processing (Sun, D.-W., Ed.). Academic Press, 2005, pp.353-386, ISBN: 0-12-676757-2.
Lawrie, R. A. Chapter 9 – The Storage and Preservation of Meat: III Direct microbial inhibition. In: Lawrie’s Meat Science (Seventh Edition) (R.A. Lawrie, D. A. Ledward, Eds.). Woodhead Publishing Series in Food Science, Technology and Nutrition, 2006, pp. 264-278, Print ISBN: 9781845691592, eBook ISBN: 9781845691615. https://doi.org/10.1533/9781845691615.264.
Lee, Y., Song, K.B. Effect of gamma-irradiation on the molecular properties of myoglobin. Journal of Biochemistry and Molecular Biology, 2002, 35(6):590-4. https://doi.org/10.5483/bmbrep.2002.35.6.590.
Mancini R., Hunt M. Current research in meat color. Meat Science, 2005,71:100–121. https://doi.org/10.1016/j.meatsci.2005.03.003.
Millar, S. J., Moss, B. W., MacDougall, D. B., Stevenson, M. H. The effect of radiation on the CIELAB colour co-ordinates of chicken breast meat as measured by different instruments. International Journal of Food Science and Technology, 1995, 30(5): 663–674. https://10.1111/j.1365-2621.1995.tb01413.x.
Nanke, K. E. Effects of ionizing radiation on pork, beef, and turkey quality. PhD thesis by Iowa State University, USA, 1998.
Nisar, M. F., Arshad, M. S., Yasin, M., Khan, M. K., Afzaal, M., Sattar, S., Suleria, H. A. R. Evaluation of gamma irradiation and moringa leaf powder on quality characteristics of meat balls under different packaging materials. Journal of Food Processing and Preservation, 2020, 44(10): e14748.https://doi.org/10.1111/jfpp.14748.
OECD Data, 2021 https://data.oecd.org/. Rima, F., Sadakuzzaman, M., Hossain, M., Ali, M., Hashem, M. Effect of gamma irradiation on shelf life and quality of Broiler meat. SAARC Journal of Agriculture, 2019, 17(1), 149–159. https://doi.org/10.3329/sja.v17i1.42768.
Rodrigues, L.M., Sales, L.A., Fontes, P.R., Torres Filho, R.A., Andrade, M.P.D., Ramos, A.L.S., Ramos, E.M. Combined effects of gamma irradiation and aging on tenderness and quality of beef from Nellore cattle. Food Chemistry, 2020,313:126137. https://doi.org/10.1016/j.foodchem.2019.126137.
Satterlee, L.D., Brown, W.D., Lycometros, C. Stability and characteristics of the pigment produced by gamma irradiation of metmyoglobin. Journal of Food Science, 1972, 37: 213-217.https://doi.org/10.1111/j.1365-2621.1972.tb05819.x
Shankar, S., Karboune, S., Salmieri, S., Lacroix, M. Development of antimicrobial formulation based on essential oils and gamma irradiation to increase the shelf life of boneless chicken thighs. Radiation Physics and Chemistry, 2022, 192:109893. https://doi.org/10.1016/j.radphyschem.2021.109893.
Sebranek, J. G., Dikeman, M., Devine, C. E. Irradiation. In: Encyclopedia of Meat Sciences (Second Edition) (M. Dekeman, C. Devine, Eds.). Academic Press, 2014. Pp. 140-144, https://doi.org/10.1016/B978-0-12-384731-7.00135-5.
Sedeh, F. M., Arbabi, K., Fatolahi, H., Abhari, M. Using gamma irradiation and low temperature on microbial decontamination of red meat in Iran. Indian journal of microbiology, 2007, 47(1): 72–76. https://doi.org/10.1007/s12088-007-0013-y
Sørheim, O., Nissen, H., Nesbakken, T., The storage life of beef and pork packaged in an atmosphere with low carbon monoxide and high carbon dioxide. Meat Science,1999, 52: 157-164.https://doi.org/10.1016/S0309-1740(98)00163- 6.
Torgby-Tetteh, W., Adu-Gyamfi, A., Odai, B.T., Appiah, V. Combined effect of irradiation and frozen storage on survival of viable bacteria and inoculated Escherichia Coli in chicken. Journal of Food and Nutrition Sciences, 2014, 2 (3): 53-57. https://doi.org/10.11648/j.jfns.20140203.11.
Xiao, S., Zhang, W. G., Lee, E. J., Ma, C. W., Ahn, D. U. Effects of diet, packaging, and irradiation on protein oxidation, lipid oxidation, and color of raw broiler thigh meat during refrigerated storage. Poultry Science, 2011, 90(6): 1348–1357. https://doi.org/10.3382/ps.2010-01244.
Zhou, G.H., Xu, X.L., Liu, Y. Preservation technologies for fresh meat – A review. Meat Science, 2010, 86: 119-128.https://doi.org/10.1016/j.meatsci.2010.04.033
Arshad, M. S., Amjad, Z., Yasin, M., Saeed, F., Imran, A., Sohaib, M., Anjum, F. M., Hussain, S. Quality and stability evaluation of chicken meat treated with gamma irradiation and turmeric powder. International Journal of Food Properties, 2019, 22 (1): 154-172. https://doi.org/10.1080/10942912.2019.1575395.
Arvanitoyannis, I., Tserkezou, P. Legislation on Food Irradiation (EU, US, Canada, Australia, Brazil). In: Irradiation of Food Commodities (I. Arvanitoyanis, Ed.). Academic Press, 2010, pp. 3-20.https://doi.org/10.1016/B978-0-12-374718 1.10001-X.
Balamatsia, C.C., Rogga, K., Badeka, A., Kontominas, M.G., Savvaidis, I.N. Effect of low-dose radiation on microbiological, chemical, and sensory characteristics of chicken meat stored aerobically at 4 degrees C. Journal of Food Protection, 2006, 69(5):1126-1133.https://doi.org/10.4315/0362-028x-69.5.1126.
Bhoir, S. A., Jhaveri, M., Chawla, S. P. (2019). Evaluation and predictive modeling of the effect of chitosan and gamma irradiation on quality of stored chilled chicken meat. Journal of Food Process Engineering, 2019, 42(7): e13254.https://doi.org/10.1111/jfpe.13254.
Borenstein, M., Hedges, L. V., Higgins, J. P. T., Rothstein, H. R. Introduction to meta-analysis. Chichester, UK: John Wiley & Sons, Ltd., 2009.
Borenstein, M., Hedges, L. V., Higgins, J. P. T., Rothstein, H. R. A basic introduction to fixed-effect and random-effects models in meta-analysis. Research Synthesis Methods, 2010, 1: 97-111.https://doi.org/10.1002/jrsm.12.
Brewer, S. (2004). Irradiation effects on meat color – a review. Meat Science, 2004, 68(1): 1–17. https://10.1016/j.meatsci.2004.02
Carriquiry, M., Weber, W. J.,Crooker, B. A. Administration of bovine somatotropin in early lactation: A meta-analysis of production responses by multiparous Holstein cows. Journal of Dairy Science, 2008, 91, 2641–2652.https://doi.org/10.3168/jds.2007-0841.
Chouliara, E., Badeka, A., Savvaidis, I., Kontominas, M. G. Combined effect of irradiation and modified atmosphere packaging on shelf-life extension of chicken breast meat: microbiological, chemical and sensory changes. European Food Research and Technology, 2007, 226(4), 877–888.https://doi.org/10.1007/s00217-007-0610-3.
Correa, W., Brandenburg, J., Behrends, J., Heinbockel, L., Reiling, N., Paulowski, L., Schwudke, D., Stephan,K., Martinez-de-Tejada, G., Brandenburg, K., Gutsmann, T. Inactivation of bacteria by γ-irradiation to investigate the interaction with antimicrobial peptides, Biophysical Journal, 2019, 117 (10): 1805-1819. https://doi.org/10.1016/j.bpj.2019.10.012.
DeCoster, J. Meta-Analysis Notes, 2009. Retrieved on 12.03.2022 from http://www.stat-help.com/notes.html.
Dourou, D., Spyrelli, E. D., Doulgeraki, A. I., Argyri, A. A., Grounta, A., Nychas, G. E., Chorianopoulos, N. G., Tassou, C. C. Microbiota of chicken breast and thigh fillets stored under different refrigeration temperatures assessed by next-generation sequencing. Foods (Basel, Switzerland), 2021,10(4): 765. https://doi.org/10.3390/foods10040765.
Erkmen, O., Bozoglu, T.F. Food Preservation by low temperatures. Food Microbiology: Principles into Practice, 2016, 34–43. https://doi.org/10.1002/9781119237860.ch29.
Fernandez-Duque, E. Comparing and combining data across studies: alternatives to significance testing. Oikos, 1997, 79(3):616.https://doi.org/10.2307/3546906.
Furuta, M., Dohmaru, T., Katayama, T., Toratani, H., Takeda, A. Detection of irradiated frozen meat and poultry using carbon monoxide gas as a probe. Journal of Agricultural and Food Chemistry,1992, 40(7): 1099–1100.https://doi.org/10.1021/jf00019a001.
Gonçalves-Tenório, A., Silva, B. N., Rodrigues, V., Cadavez, V., Gonzales-Barron, U. Prevalence of Pathogens in Poultry Meat: A Meta-Analysis of European Published Surveys. Foods (Basel, Switzerland), 2018, 7(5): 69. https://doi.org/10.3390/foods7050069
Higgins, J. P. T., Thompson, S. G. Quantifying heterogeneity in meta-analysis. Statistics in Medicine, 2002, 21: 1539–1558.https://doi.org/10.1002/sim.1186.
Islam, A., Sadakuzzaman, M., Hossain, M. A., Hossain, M. M., Hashem, M. A. Effect of gamma irradiation on shelf life and quality of indigenous chicken meat: Irradiation on chicken meat. Journal of the Bangladesh Agricultural University, 2019, 17(4): 560–566. https://doi.org/10.3329/jbau.v17i4.44626.
Javanmard, M., Rokni, N., Bokaie, S., Shahhosseini, G. Effects of gamma irradiation and frozen storage on microbial, chemical and sensory quality of chicken meat in Iran. Food Control, 2006, 17(6): 469-473.https://doi.org/10.1016/j.foodcont.2005.02.008.
Kanatt, S. R., Chawla, S. P., Sharma, A. (2015). Effect of radiation processing on meat tenderization. Radiation Physics and Chemistry, 2015,111:1–8. https://doi.org/10.1016/j.radphyschem.2015.02.004
Khalid, W., Arshad, M. S., Yasin, M., Imran, A., Ahmad, M. H. Quality characteristics of gamma irradiation and kale eaf powder treated ostrich and chicken meat during storage. International Journal of Food Properties, 2021, 24:1, 1335-1348. https://doi.org/10.1080/10942912.2021.1963274.
Kralik, G.,Kralik, Z., Grčević, M., Hanžek, D. Quality of chicken meat. In: Animal Husbandry and Nutrition (B. Yücel, T. Taşkin, Eds). IntechOpen, London, 2017. https://doi.org/10.5772/intechopen.72865.
Lacroix, M. Irradiation of foods. In: Emerging Technologies for Food Processing (Sun, D.-W., Ed.). Academic Press, 2005, pp.353-386, ISBN: 0-12-676757-2.
Lawrie, R. A. Chapter 9 – The Storage and Preservation of Meat: III Direct microbial inhibition. In: Lawrie’s Meat Science (Seventh Edition) (R.A. Lawrie, D. A. Ledward, Eds.). Woodhead Publishing Series in Food Science, Technology and Nutrition, 2006, pp. 264-278, Print ISBN: 9781845691592, eBook ISBN: 9781845691615. https://doi.org/10.1533/9781845691615.264.
Lee, Y., Song, K.B. Effect of gamma-irradiation on the molecular properties of myoglobin. Journal of Biochemistry and Molecular Biology, 2002, 35(6):590-4. https://doi.org/10.5483/bmbrep.2002.35.6.590.
Mancini R., Hunt M. Current research in meat color. Meat Science, 2005,71:100–121. https://doi.org/10.1016/j.meatsci.2005.03.003.
Millar, S. J., Moss, B. W., MacDougall, D. B., Stevenson, M. H. The effect of radiation on the CIELAB colour co-ordinates of chicken breast meat as measured by different instruments. International Journal of Food Science and Technology, 1995, 30(5): 663–674. https://10.1111/j.1365-2621.1995.tb01413.x.
Nanke, K. E. Effects of ionizing radiation on pork, beef, and turkey quality. PhD thesis by Iowa State University, USA, 1998.
Nisar, M. F., Arshad, M. S., Yasin, M., Khan, M. K., Afzaal, M., Sattar, S., Suleria, H. A. R. Evaluation of gamma irradiation and moringa leaf powder on quality characteristics of meat balls under different packaging materials. Journal of Food Processing and Preservation, 2020, 44(10): e14748.https://doi.org/10.1111/jfpp.14748.
OECD Data, 2021 https://data.oecd.org/. Rima, F., Sadakuzzaman, M., Hossain, M., Ali, M., Hashem, M. Effect of gamma irradiation on shelf life and quality of Broiler meat. SAARC Journal of Agriculture, 2019, 17(1), 149–159. https://doi.org/10.3329/sja.v17i1.42768.
Rodrigues, L.M., Sales, L.A., Fontes, P.R., Torres Filho, R.A., Andrade, M.P.D., Ramos, A.L.S., Ramos, E.M. Combined effects of gamma irradiation and aging on tenderness and quality of beef from Nellore cattle. Food Chemistry, 2020,313:126137. https://doi.org/10.1016/j.foodchem.2019.126137.
Satterlee, L.D., Brown, W.D., Lycometros, C. Stability and characteristics of the pigment produced by gamma irradiation of metmyoglobin. Journal of Food Science, 1972, 37: 213-217.https://doi.org/10.1111/j.1365-2621.1972.tb05819.x
Shankar, S., Karboune, S., Salmieri, S., Lacroix, M. Development of antimicrobial formulation based on essential oils and gamma irradiation to increase the shelf life of boneless chicken thighs. Radiation Physics and Chemistry, 2022, 192:109893. https://doi.org/10.1016/j.radphyschem.2021.109893.
Sebranek, J. G., Dikeman, M., Devine, C. E. Irradiation. In: Encyclopedia of Meat Sciences (Second Edition) (M. Dekeman, C. Devine, Eds.). Academic Press, 2014. Pp. 140-144, https://doi.org/10.1016/B978-0-12-384731-7.00135-5.
Sedeh, F. M., Arbabi, K., Fatolahi, H., Abhari, M. Using gamma irradiation and low temperature on microbial decontamination of red meat in Iran. Indian journal of microbiology, 2007, 47(1): 72–76. https://doi.org/10.1007/s12088-007-0013-y
Sørheim, O., Nissen, H., Nesbakken, T., The storage life of beef and pork packaged in an atmosphere with low carbon monoxide and high carbon dioxide. Meat Science,1999, 52: 157-164.https://doi.org/10.1016/S0309-1740(98)00163- 6.
Torgby-Tetteh, W., Adu-Gyamfi, A., Odai, B.T., Appiah, V. Combined effect of irradiation and frozen storage on survival of viable bacteria and inoculated Escherichia Coli in chicken. Journal of Food and Nutrition Sciences, 2014, 2 (3): 53-57. https://doi.org/10.11648/j.jfns.20140203.11.
Xiao, S., Zhang, W. G., Lee, E. J., Ma, C. W., Ahn, D. U. Effects of diet, packaging, and irradiation on protein oxidation, lipid oxidation, and color of raw broiler thigh meat during refrigerated storage. Poultry Science, 2011, 90(6): 1348–1357. https://doi.org/10.3382/ps.2010-01244.
Zhou, G.H., Xu, X.L., Liu, Y. Preservation technologies for fresh meat – A review. Meat Science, 2010, 86: 119-128.https://doi.org/10.1016/j.meatsci.2010.04.033
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How to Cite
DIMOV, Krasimir; POPOVA, Teodora.
A meta-analysis of the effect of gamma irradiation on chicken meat quality: Microbiology and colour.
Food Science and Applied Biotechnology, [S.l.], v. 5, n. 2, p. 160-172, oct. 2022.
ISSN 2603-3380.
Available at: <https://www.ijfsab.com/index.php/fsab/article/view/185>. Date accessed: 21 mar. 2025.
doi: https://doi.org/10.30721/fsab2022.v5.i2.185.