Tackling food spoilage bacteria: How pomegranate peel extract can improve beef safety
Main Article Content
Keywords
Beef product, food spoilage, pomegranate peel extract, Pseudomonas aeruginosa, natural preservatives
Abstract
Meat is among the most popular foods because of its high dietary component. However, it is contaminated with various food spoilage bacteria, including Pseudomonas aeruginosa, identified as a primary contributor to food spoilage and foodborne illnesses. This investigation evaluates the total aerobic and psychrotrophic counts, antibacterial resistance, and virulence features in P. aeruginosa bacteria discovered in 150 beef products. Thirty each of basterma, hot dogs, luncheon, frankfort, and burgers were obtained from numerous markets in El-Fayoum Governorate, Egypt, using culture and molecular techniques. Furthermore, the influence of pomegranate peel (PP) extract on marinated beef steak was evaluated in vitro during the storage period. Burger samples recorded the greatest total aerobic count (TAC) and psychrotrophic count (5.52 ± 2.5 and 3.88 ± 2.1 log CFU/g, respectively), while basterma samples had the lowest count (3.37 ± 2.1 and 1.89 ± 1.3 log CFU/g, respectively). Furthermore, P. aeruginosa contaminated 32.7% of the samples. Burger and hot dog samples had the greatest isolation percentage (46.7% and 36.7%, respectively), while basterma samples had the lowest proportions (20%). In addition, the mean P. aeruginosa count extended from 1.80 ± 1.1 log CFU/g (basterma) to 4.91 ± 1.3 log CFU/g (burger). PCR results of the 16S rRNA gene at 150 bp exhibited that P. aeruginosa DNA was present in all of the suspected isolates. The virulence genes pilB (14.3%), PslA (18.4%), toxR (14.3%), and exoS (10.2%) were the most common ones found. High resistance rates were observed toward ampicillin and tetracycline (100%) and complete susceptibility to florfenicol and ciprofloxacin, making them the most significant antibiotics. Using 25%, 50%, 75%, and 100% PP extract solutions, respectively, reduced the P. aeruginosa count in the assessed samples over 48 h by 32.44%, 32.96%, 49.63%, and 52.11%. In addition, the investigation verified the group submerged in a 75% PP extract solution had better sensory criteria, which greatly varied from the control and other treatment groups.
References
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Jurado-Martín I., Sainz-Mejías M., McClean S. 2021. Pseudomonas aeruginosa: An audacious pathogen with an adaptable arsenal of virulence factors. Int. J. Mol. Sci. 22:3128. 10.3390/ijms22063128
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Khairy E.N., Al-Qaaneh A.M., Mounir M.B., Abdelhaseib M., Reda A.G., Ali M.A., et al. 2024. Citrus reticulata flavonoids as a valuable source for reducing meat-borne Aeromonas hydrophila. Italian J. Food Sci. 36(3):263–273. 10.15586/ijfs.v36i3.2606.
Khan M., Stapleton F., Summers S., Rice S.A., Willcox M.D. 2020. Antibiotic resistance characteristics of Pseudomonas aeruginosa isolated from keratitis in Australia and India. Antibiotics (Basel, Switzerland). 9:600. 10.3390/antibiotics9090600
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Lozano C., López M., Rojo-Bezares B., Sáenz Y. 2020. Antimicrobial susceptibility testing in Pseudomonas aeruginosa biofilms: One step closer to a standardized method. Antibiotics (Basel). 9:880. 10.3390/antibiotics9120880
Makharita R.R., Iman M.A., Helal F.H., Mohamed H., Fatma I.H., Amera A., et al. 2020. Antibiogram and genetic characterization of carbapenem-resistant gram-negative pathogens incriminated in healthcare-associated infections. Infec. Drug Resist. 13:3991–4002. 10.2147/IDR.S276975
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Nady K., Abdelmotilib N.M., Salem-Bekhit M.M., Salem M.M., Singh S., Dandrawy M.K. 2024. Antibacterial efficiency of apple vinegar marination on beef-borne Salmonella. Open Vet. J. 14(1):274–283. 10.5455/OVJ.2024.v14.i1.24
Nikbin V.S., Aslani M.M., Sharafi Z., Hashemipour M., Shahcheraghi F., Ebrahimipour G.H. 2012. Molecular identification and detection of virulence genes among Pseudomonas aeruginosa isolated from different infectious origins. Iran. J. Microbiol. 4:118–123.
Poursina S., Ahmadi M., Fazeli F., Ariaii P. 2023. Assessment of virulence factors and antimicrobial resistance among the Pseudomonas aeruginosa strains isolated from animal meat and carcass samples. Vet. Med. Sci. 9:315–325. 10.1002/vms3.1007
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Ragab A.Y., Abobakr M.E., Fahim A.E., Amani M.S. 2022. Effect of titanium dioxide nanoparticles and thyme essential oil on the quality of the chicken fillet. BVMJ. 41:38–40. 10.21608/bvmj.2021.107456.1488
Rasuli N., Bintoro V.P., Purnomoadi A., Nurwantoro N. 2021. The shelf life of buffalo meat marinated with pomegranate (Punica granatum) peel extract. J. Adv. Vet. Anim. Res. 8:612–618. 10.5455/javar.2021.h552
Rather I.A., Koh W.Y., Paek W.K., Lim, J. 2017. The sources of chemical contaminants in food and their health implications. Front. Pharm. 8:1–8. 10.3389/fphar.2017.00830
Rezaloo M., Abbasali M., Zohreh M., Amirali A. 2022. Prevalence, antimicrobial resistance, and molecular description of Pseudomonas aeruginosa isolated from meat and meat products. J. Food Qual. 9899338:11. 10.1155/2022/9899338
Rosas-Burgos E.C., Burgos-Hernández A., Noguera-Artiaga L., Kačániová M., Hernández-García F., Cárdenas-López J.L., et al. 2017. Antimicrobial activity of pomegranate peel extracts as affected by cultivar. J. Sci. Food Agr. 97(3):802–810. 10.1002/jsfa.7799
Rostamzadeh Z., Mohammadian M., Rostamzade A. 2016. Investigation of Pseudomonas aeruginosa resistance pattern against antibiotics in clinical samples from Iranian educational hospital. Adv. Microbiol. 6:190–194. 10.4236/aim.2016.63019
Salem A., Osman I., Shehata S. 2018. Assessment of psychrotrophic bacteria in frozen fish with special reference to Pseudomonas spp. BVMJ. 34:140–148. 10.21608/bvmj.2018.29423
Sattar A., Abbas A.S., Naseem S., Mumtaz M., Shabbir A., Mirza S.S. 2024. Evaluation of phytochemicals and antibacterial usefulness of citrus limon & cicer arietinum in synergistic effect with antibiotics against clinically important bacteria. J. Health Reh. Res. 4:244–249. 10.61919/jhrr.v4i1.174
Sengun I.Y., Goztepe E., Ozturk B. 2019. Efficiency of marination liquids prepared with koruk (Vitis vinifera L.) on safety and some quality attributes of poultry meat. LWT. 113:108317. 10.1016/j.lwt.2019.108317
Shahrokhi G.R., Rahimi E., Shakerian A. 2022. The prevalence rate, pattern of antibiotic resistance, and frequency of virulence factors of Pseudomonas aeruginosa strains isolated from fish in Iran. J. Food Qual. 8990912:8. 10.1155/2022/8990912
Shaltout F.A., Ahmed A., Ibrahim A.E., Ahmed Y.A. 2016. Prevalence of some foodborne microorganisms in meat and meat products. BVMJ. 31:213–219. 10.21608/bvmj.2016.31300
Sheir S.H., Ibrahim H., Hassan M., Shawky N. 2020. Incidence of psychotropic bacteria in frozen chicken meat products with special reference to Pseudomonas species. BVMJ. 39:165–168. 10.21608/bvmj.2020.37744.1238
Sofy A.R., Sharaf A.E., Al Karim A.G., Hmed A.A., Moharam K.M. 2017. Prevalence of the harmful Gram-negative bacteria in ready-to-eat foods in Egypt. Food Publ. Heal. 7(3):59–68. 10.5923/j.fph.20170703.02
SPSS for Windows. 2001. Version: 11 (19 September 2001). Chicago, IL: Copyright SPSS Inc. 1989–2001
Tartor Y.H., and El-naenaeey E.Y. 2016. RTPCR detection of exotoxin genes expression in multidrug-resistant Pseudomonas aeruginosa. J. Mol. Cell Biol. 62:56–62. 10.14715/cmb/2016.62.1.11
Wang Z., Pan Z., Ma H., Atungulu G.G. 2011. Extract of phenolics from pomegranate peels. Open Food Sci. J. 5:17–25. 10.2174/1874256401105010017
Wang G.Y., Wang H.H., Han Y.W., Xing T., Ye K. P., Xu X.L., et al. 2017. Evaluation of the spoilage potential of bacteria isolated from chilled chicken in vitro and in situ. Food Microbial. 63:139–146. 10.1016/j.fm.2016.11.015
Wang X., Wang Z., Sun Z., Wang D., Liu F., Lin L. 2023. In vitro and in situ characterization of psychrotrophic spoilage bacteria recovered from chilled chicken. Foods. 12:95. 10.3390/foods12010095
Wang Y., Chen X., Whalen J.K., Cao Y., Quan Z., Lu C., et al. 2015. Kinetics of inorganic and organic phosphorus release influenced by low molecular weight organic acids in calcareous, neutral and acidic soils. J. Plant Nutr. Soil SC. 178(4):555–66. 10.1002/jpln.201500047
WHO. 2022. World Health Organization. Global antimicrobial resistance and use surveillance system (GLASS) report: 2022 (No. 9789240062702). www.who.int/news-room/fact-sheets/detail/food-safety
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Akuru E.A., Oyeagu C.E., Mpendulo T.C., Rautenbach F., Oguntibeju O.O. 2020. Effect of pomegranate (Punica granatum L) peel powder meal dietary supplementation on antioxidant status and quality of breast meat in broilers. Heliyon. 6:e05709. 10.1016/j.heliyon.2020.e05709
Algammal A., Mabrok M., Sivaramasamy E., Youssef F., Atwa M., Wahdan A., et al. 2020. Emerging MDR-Pseudomonas aeruginosa in fish commonly harbor oprL and toxA virulence genes and blaTEM, blaCTX-M, and tetA antibiotic-resistance genes. Sci. Rep. 10:1–12. 10.1038/s41598-020-72264-4
Al-Hadidy Y., Oleiwi S., Khalaf A., Saleh H. 2023. The effectiveness of adding apple cider vinegar and garlic to chicken meat kebabs as an antimicrobial and its role in improving its sensory and physiochemical properties. Kirkuk. Univ. J. Agr. Sci. 14:117–130. 10.58928/ku23.14110
Al-Mutairi M.F. 2011. The incidence of Enterobacteriaceae causing food poisoning in some meat products. Adv. J. Food Sci. Tech. 3:116–121
Benie C.K., Dadié A., Guessennd N., N’gbesso-Kouadio N.A., Kouame N.D., N’golo D.C., et al. 2017. Characterization of virulence potential of Pseudomonas Aeruginosa isolated from bovine meat, fresh fish, and smoked fish. Eur J Microbiol Immunol (Bp). 7(1):55–64. 10.1556/1886.2016.00039
Caldera L., Franzetti L., Van-Coillie E. 2016. Identification, enzymatic spoilage characterization and proteolytic activity quantification of Pseudomonas spp. isolated from different foods. Food Microbiol. 54:142–53. 10.1016/j.fm.2015.10.004
CLSI. Clinical and Laboratory Standards Institute. 2021. L.S. Methods for antimicrobial disk susceptibility testing of bacteria isolated from aquatic animals. M100-ED29: Performance standards for antimicrobial susceptibility testing CLSI. 40:50–51. https://www.nih.org.pk/wpcontent/uploads/2021/02/CLSI-2020.pdf
Elbarbary N., Dandrawy M.K., Hadad G., Abdelhaseib M., Amna A., Alenazy R., et al. 2024. Bacterial quality and molecular detection of food poisoning virulence genes isolated from Nasser Lake fish, Aswan, Egypt. Int. J. Food Sci. 6095430:12. 10.1155/2024/6095430
El-Hadary A.E., and Taha M. 2020. Pomegranate peel methanolic-extract improves the shelf-life of edible-oils under accelerated oxidation conditions. Food Sci. Nutr. 8:1798–1811. 10.1002/fsn3.1391
EOS. 2005/1042. Egyptian Standards No. for basterma, Organization for Standardization and quality, Arab Republic of Egypt.
EOS. 2005/1114. Egyptian Standards for beef luncheon, Egyptian Organization for Standardization and quality, Arab Republic of Egypt.
EOS. 2005/1688. Egyptian Standards for beef burger, Egyptian Organization for Standardization and quality, Arab Republic of Egypt.
EOS. 2005/3492. Egyptian Standards for hot dog and frankfort, Egyptian Organization for Standardization and quality, Arab Republic of Egypt.
Ghadaksaz A., Abbas A.I., Hamideh M.H., Mohsen A. 2015. The prevalence of some Pseudomonas virulence genes related to biofilm formation and alginate production among clinical isolates. J. Appl. Biom. 13:61–68. 10.1016/j.jab.2014.05.002
Habeeb R.H., Saad S.N., Al-Jubory A. 2012. A study of efficacy of disinfectants and bacterial contamination in Alhilla teaching hospital. Med. J. Babyl. 9:890–900.
Hamed E.A., Ahmed A.S., Abd El-Aaty M.F. 2015. Bacteriological hazard associated with meat and meat products. Egypt. J. Agr. Res. 93:385–393.
Hamisi Z., Tuntufye H., Shahada F. 2012. Antimicrobial resistance phenotypes of Escherichia coli isolated from tropical free-range chickens. Int. J. Sci. Res. 3:34. https://www.ijsr.net/archive/v3i9/MDIwMTU3Nw==.pdf
Hayrapetyan H., Hazeleger W.C., Beumer R.R. 2012. Inhibition of Listeria monocytogenes by pomegranate (Punica granatum) peel extract in meat paté at different temperatures. Food Cont. 23:66–72. 10.1016/j.foodcont.2011.06.012
Ibrahim H.M., Reham A., Nesreen Z., Ghanaym H.R. 2018. Effect of marination on Vibrio Parahaemolyticus in Tilapia Fillets. Benha Vet. Med. J. 34:234–245. 10.21608/bvmj.2018.29434
Jurado-Martín I., Sainz-Mejías M., McClean S. 2021. Pseudomonas aeruginosa: An audacious pathogen with an adaptable arsenal of virulence factors. Int. J. Mol. Sci. 22:3128. 10.3390/ijms22063128
Khairy E.N., Morshdy A.E.M., Abdelmotilib N.M., Gomaa R.A., Zaki R.S. 2023. Probiotics blueprint for meliorating the quality aspects of chicken nuggets. J. Adv. Vet. Res. 13(10):1960–1965. https://www.advetresearch.com/index.php/AVR/article/view/1587
Khairy E.N., Al-Qaaneh A.M., Mounir M.B., Abdelhaseib M., Reda A.G., Ali M.A., et al. 2024. Citrus reticulata flavonoids as a valuable source for reducing meat-borne Aeromonas hydrophila. Italian J. Food Sci. 36(3):263–273. 10.15586/ijfs.v36i3.2606.
Khan M., Stapleton F., Summers S., Rice S.A., Willcox M.D. 2020. Antibiotic resistance characteristics of Pseudomonas aeruginosa isolated from keratitis in Australia and India. Antibiotics (Basel, Switzerland). 9:600. 10.3390/antibiotics9090600
Kilinc B., and Cakli S. 2004. Chemical, microbiological and sensory changes in thawed frozen fillets of Sardine (Sardina pilchardus) during marination. Food Chem. 88:275–280. 10.1016/j.foodchem.2004.01.044
Lozano C., López M., Rojo-Bezares B., Sáenz Y. 2020. Antimicrobial susceptibility testing in Pseudomonas aeruginosa biofilms: One step closer to a standardized method. Antibiotics (Basel). 9:880. 10.3390/antibiotics9120880
Makharita R.R., Iman M.A., Helal F.H., Mohamed H., Fatma I.H., Amera A., et al. 2020. Antibiogram and genetic characterization of carbapenem-resistant gram-negative pathogens incriminated in healthcare-associated infections. Infec. Drug Resist. 13:3991–4002. 10.2147/IDR.S276975
Meng L., Liu H., Lan T., Dong L., Hu H., Zhao S., et al. 2020. Antibiotic resistance patterns of Pseudomonas spp. isolated from raw milk revealed by whole genome sequencing. Front. Microbial. 11:1005. 10.3389/fmicb.2020.01005
Nady K., Abdelmotilib N.M., Salem-Bekhit M.M., Salem M.M., Singh S., Dandrawy M.K. 2024. Antibacterial efficiency of apple vinegar marination on beef-borne Salmonella. Open Vet. J. 14(1):274–283. 10.5455/OVJ.2024.v14.i1.24
Nikbin V.S., Aslani M.M., Sharafi Z., Hashemipour M., Shahcheraghi F., Ebrahimipour G.H. 2012. Molecular identification and detection of virulence genes among Pseudomonas aeruginosa isolated from different infectious origins. Iran. J. Microbiol. 4:118–123.
Poursina S., Ahmadi M., Fazeli F., Ariaii P. 2023. Assessment of virulence factors and antimicrobial resistance among the Pseudomonas aeruginosa strains isolated from animal meat and carcass samples. Vet. Med. Sci. 9:315–325. 10.1002/vms3.1007
Purohit H.J., Raje D.V., Kapley A. 2003. Identification of signature and primers specific to genus Pseudomonas using mismatched patterns of 16S rDNA sequences. BMC Bioinf. 4:19. 10.1186/1471-2105-4-19
Qenawy E.M., Abou-Ellail M., Abdel-Motaal F., Alshaharni M.O., Elbarbary N.K. 2024. Prevalence of Pseudomonas aeruginosa, Escherichia coli, and their virulence genes in adulterated meat products. Adv. Anim. Vet. Sci. 12:139–149. 10.17582/journal.aavs/2024/12.s1.139.149
Quinn P.J., Carter M.E., Markey B., Carter G.R. 2002. Clinical veterinary microbiology. Harcourt Publishers, Virginia. 2:331–344. https://www.scirp.org/reference/referencespapers?referenceid=2556972
Ragab A.Y., Abobakr M.E., Fahim A.E., Amani M.S. 2022. Effect of titanium dioxide nanoparticles and thyme essential oil on the quality of the chicken fillet. BVMJ. 41:38–40. 10.21608/bvmj.2021.107456.1488
Rasuli N., Bintoro V.P., Purnomoadi A., Nurwantoro N. 2021. The shelf life of buffalo meat marinated with pomegranate (Punica granatum) peel extract. J. Adv. Vet. Anim. Res. 8:612–618. 10.5455/javar.2021.h552
Rather I.A., Koh W.Y., Paek W.K., Lim, J. 2017. The sources of chemical contaminants in food and their health implications. Front. Pharm. 8:1–8. 10.3389/fphar.2017.00830
Rezaloo M., Abbasali M., Zohreh M., Amirali A. 2022. Prevalence, antimicrobial resistance, and molecular description of Pseudomonas aeruginosa isolated from meat and meat products. J. Food Qual. 9899338:11. 10.1155/2022/9899338
Rosas-Burgos E.C., Burgos-Hernández A., Noguera-Artiaga L., Kačániová M., Hernández-García F., Cárdenas-López J.L., et al. 2017. Antimicrobial activity of pomegranate peel extracts as affected by cultivar. J. Sci. Food Agr. 97(3):802–810. 10.1002/jsfa.7799
Rostamzadeh Z., Mohammadian M., Rostamzade A. 2016. Investigation of Pseudomonas aeruginosa resistance pattern against antibiotics in clinical samples from Iranian educational hospital. Adv. Microbiol. 6:190–194. 10.4236/aim.2016.63019
Salem A., Osman I., Shehata S. 2018. Assessment of psychrotrophic bacteria in frozen fish with special reference to Pseudomonas spp. BVMJ. 34:140–148. 10.21608/bvmj.2018.29423
Sattar A., Abbas A.S., Naseem S., Mumtaz M., Shabbir A., Mirza S.S. 2024. Evaluation of phytochemicals and antibacterial usefulness of citrus limon & cicer arietinum in synergistic effect with antibiotics against clinically important bacteria. J. Health Reh. Res. 4:244–249. 10.61919/jhrr.v4i1.174
Sengun I.Y., Goztepe E., Ozturk B. 2019. Efficiency of marination liquids prepared with koruk (Vitis vinifera L.) on safety and some quality attributes of poultry meat. LWT. 113:108317. 10.1016/j.lwt.2019.108317
Shahrokhi G.R., Rahimi E., Shakerian A. 2022. The prevalence rate, pattern of antibiotic resistance, and frequency of virulence factors of Pseudomonas aeruginosa strains isolated from fish in Iran. J. Food Qual. 8990912:8. 10.1155/2022/8990912
Shaltout F.A., Ahmed A., Ibrahim A.E., Ahmed Y.A. 2016. Prevalence of some foodborne microorganisms in meat and meat products. BVMJ. 31:213–219. 10.21608/bvmj.2016.31300
Sheir S.H., Ibrahim H., Hassan M., Shawky N. 2020. Incidence of psychotropic bacteria in frozen chicken meat products with special reference to Pseudomonas species. BVMJ. 39:165–168. 10.21608/bvmj.2020.37744.1238
Sofy A.R., Sharaf A.E., Al Karim A.G., Hmed A.A., Moharam K.M. 2017. Prevalence of the harmful Gram-negative bacteria in ready-to-eat foods in Egypt. Food Publ. Heal. 7(3):59–68. 10.5923/j.fph.20170703.02
SPSS for Windows. 2001. Version: 11 (19 September 2001). Chicago, IL: Copyright SPSS Inc. 1989–2001
Tartor Y.H., and El-naenaeey E.Y. 2016. RTPCR detection of exotoxin genes expression in multidrug-resistant Pseudomonas aeruginosa. J. Mol. Cell Biol. 62:56–62. 10.14715/cmb/2016.62.1.11
Wang Z., Pan Z., Ma H., Atungulu G.G. 2011. Extract of phenolics from pomegranate peels. Open Food Sci. J. 5:17–25. 10.2174/1874256401105010017
Wang G.Y., Wang H.H., Han Y.W., Xing T., Ye K. P., Xu X.L., et al. 2017. Evaluation of the spoilage potential of bacteria isolated from chilled chicken in vitro and in situ. Food Microbial. 63:139–146. 10.1016/j.fm.2016.11.015
Wang X., Wang Z., Sun Z., Wang D., Liu F., Lin L. 2023. In vitro and in situ characterization of psychrotrophic spoilage bacteria recovered from chilled chicken. Foods. 12:95. 10.3390/foods12010095
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Apr 1, 2025
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El-Hawary, S. F., Ahmed, A. M., Bekhit, M. M., Taha, E. I., Abdelhaseib, M., Abdelmotilib, N. M., Salem, M. M., & Khairy Elbarbary, N. (2025). Tackling food spoilage bacteria: How pomegranate peel extract can improve beef safety. Italian Journal of Food Science, 37(2), 228-240. https://doi.org/10.15586/ijfs.v37i2.2945
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How to Cite
El-Hawary, S. F., Ahmed, A. M., Bekhit, M. M., Taha, E. I., Abdelhaseib, M., Abdelmotilib, N. M., Salem, M. M., & Khairy Elbarbary, N. (2025). Tackling food spoilage bacteria: How pomegranate peel extract can improve beef safety. Italian Journal of Food Science, 37(2), 228-240. https://doi.org/10.15586/ijfs.v37i2.2945