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The effect of electron-beam irradiation on microbiological properties and sensory characteristics of sausages
Radiation Physics and Chemistry 168 (2020) 108524
Contents lists available at ScienceDirect
Radiation Physics and Chemistry journal homepage: www.elsevier.com/locate/radphyschem
The effect of electron-beam irradiation on microbiological properties and sensory characteristics of sausages
T
F. Bouzarjomehria, V. Dadb,c, B. Hajimohammadid, S.P. Shirmardie, A. Yousefi-Ghaleh Salimid,∗ a
Department of Medical Physics, Shahid Sadoughi University of Medical Sciences, Yazd, Iran Reference Laboratory of Water and Wastewater, Environment and Occupational Department, Shahid Sadoughi University of Medical Sciences, Yazd, Iran c Department of Microbiology, Kerman University of Medical Sciences, Kerman, Iran d Department of Food Safety and Hygiene, Faculty of Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran e Radiation Application Research School, Nuclear Science and Technology Research Institute (NSTRI), Tehran, Iran b
A R T I C LE I N FO
A B S T R A C T
Keywords: Electron treatment Salmonella typhimurium Beef sausages Sensory characteristics
The present study aimed to evaluate the survival of Salmonella typhimurium strain ATCC 14028, total bacterial populations and sensory characteristics of irradiated beef sausages. The samples were vacuum-packaged, irradiated by electron-beam, and stored in a refrigerator. Microbiological quality was promoted by irradiation dose increase. The effect of electron-beam on color, taste, odor and consistency characteristics showed no significant differences. The results indicated that using electron-beam irradiation at 2 kGy dose was a promising method in reducing bacterial populations, eliminating Salmonella typhimurium along with acceptability of sensory characteristics.
1. Introduction Nowadays, the request for ready-to-eat (RTE) and processed meat products have been increased due to their taste, convenience of use, low cost, and accessibility (Leroy and Degreef, 2015). Sausages are known as one of the most popular and delicious meats products worldwide (Sachindra et al., 2005). So far, over 2500 serotypes of Salmonella have been recognized. Approximately 2300 Salmonella strains cause salmonellosis, which is mainly characterized by abdominal pain, diarrhea, and nausea (Coburn et al., 2007). According to the Center for Disease Control (CDC) reports, among five pathogens that cause 90% of deaths, Salmonella accounts for 31% of it (Tahergorabi et al., 2012). CDC reported that 1.4 million salmonella illnesses occur annually in the U.S. which includes nearly 600 deaths and 16000 hospitalizations (Turner, 2010). The outbreaks of salmonellosis due to sausage consumption has been reported in England, Germany, France, Ireland, and the United States in 1995, 2001, 2008, 2011, 1997 and 2001, respectively (Louis Coroller et al., 2015). Electron-beam irradiation in the low-dose ionization radiation in the treatment of foods and crops could be applied for both industry and consumers interests due to eliminating microbial contamination (Lung et al., 2015). In comparison studies of electron beam irradiation on various attributes, it was effective to decrease total bacterial populations (Cambero et al., 2012) and Salmonella typhimurium (Hwang et al.,
∗
2009) in refrigerated beef. The majority of consumers are uncertain about the safety of sausages and have negative attitudes toward irradiated foods. Optimum dose irradiation with regards to sensory quality would be make the acceptance of irradiated hot dog smoked sausage. Despite high consumption with various ingredients, there is little information on the quality characteristics of irradiated hot dog smoked sausages. The objective of this study was to investigate This study aimed at evaluating the effectiveness of electron-beam irradiation in the treatment of contaminated sausages with Salmonella typhimurium, total bacterial population, and sensory characteristics. 1.1. Sample preparation and irradiation treatment The samples of hot dog smoked sausage (made from raw ground beef 70% (15% fat), with various ingredients such as starch 4.1%, ice 5%, sodium chloride 2%, sodium nitrite 0.3%, garlic 0.95%, ginger 0.95%, dextrose 0.7%, Paprika 0.5%, black pepper 0.5%) were ground for microbiological analysis. Sausages were divided into 25-g pieces and placed in vacuum bags. The vacuum-packaged sausages were packed in polyethylene box and transmitted to irradiation plant, exposed to electron-beam at the dose of 15 kGy before inoculating with Salmonella typhimurium (Fallah et al., 2010). The inoculated samples were achieved initial loads of approximately 108 C.F.U/g. The samples
Corresponding author. E-mail address: atefeh69yousefi@gmail.com (A. Yousefi-Ghaleh Salimi).
https://doi.org/10.1016/j.radphyschem.2019.108524 Received 11 November 2017; Received in revised form 30 August 2019; Accepted 10 October 2019 Available online 13 October 2019 0969-806X/ © 2019 Elsevier Ltd. All rights reserved.
Radiation Physics and Chemistry 168 (2020) 108524
F. Bouzarjomehri, et al.
were irradiated at doses of 0 (control), 1, 2, 3 and 5 kGy. The irradiated and non-irradiated samples were stored at 4 ± 0.5 °C in the refrigerator, excluding the ones which must be analyzed on day one. The samples were placed at room temperature for 50 min and analyzed for various days 0, 5, 10, 30 and 45. Fig. 1. Visual analogue scales (VAS).
1.2. Inoculum preparation
Independent sample T-test was used to determine differences at 95% confidence level.
All microbial cultures were prepared from the Merck company, Darmstadt, Germany. Salmonella enterica serotype Typhimurium ATCC 14028 was streaked onto nutrient agar, eosin methylene-blue lactose sucrose agar and mueller hinton agar and were incubated at 37 °C for 24 h. The colonies were transferred to selective enrichment broths (tryptic soy broth and nutrient broth) and incubated at 37 °C for 24 h. Then the incubated tubes (each with an equal volume) were centrifuged at 3000 g for 10 min at 20 °C. The obtained biomasses at the bottom of each tube were separated and transferred to 9 mL of buffered peptone water to acquire a population level of nearly 109 C.F.U/ml. One milliliter of the prepared suspension was transferred into irradiated (15 kGy) packages. Then, the samples were kneaded for 2 min and incubated at 35 °C for 24 h (Fallah et al., 2010).
2. Results 2.1. Microbiological properties The results for the survival of Salmonella typhimurium and total bacterial populations of beef sausages during storage at 4 °C (Fig. 1, Fig. 2). The microbiological quality of treated samples was significantly improved (p < 0.05). Salmonella typhimurium and total bacterial populations at doses of 2, 3, and 5 kGy to 3 log and at dose of 1 kGy to 0.3 and 2.2 log reduced, respectively.
1.3. Irradiation method 2.2. Sensory characteristics
Electron-beam irradiation was done in Central Processor Irradiation, Yazd, Iran. Electron-beam with 10 MeV was produced by rhodotron accelerator TT200 model (IBA, Belgium). One hundred samples in 25 gr pieces were moved at 5 m/s on a conveyor during of electron expose. Approximately, each sample was irradiated for 2 min. Doses of 0, 1, 2, 3 and 5 kGy were absorbed in each group. Dosimetry was conducted by FWT film (9F9, Goleta, CA). The absorption dose of each sample groups was: 1 ± %9, 2 ± %5, 3 ± %3, 5 ± %2.
The sensory characteristics of irradiated sausages showed no significant differences. The changes in VAS scores are represented in Fig. 3. Significant differences (to the control) in properties of color and odor (p < 0.05) were observed at 1 and 2 kGy doses, respectively. The results also indicated a significant difference (within groups) in the consistency of irradiated samples by 2 kGy dose (p < 0.05). There was a significant difference (within groups) of taste property at 0, 2 and 5 kGy doses.
1.4. Salmonella typhimurium enumeration Salmonella typhimurium was enumerated by the Most Probable Number (MPN), a method to approximate the population density of viable microorganisms. One gr of inoculated sausages were transferred to 10 mL of tetrathionate broth. These tubes were incubated at 35 °C for 24 h, and then 10, 1 and 0.1 mL of the enriched suspension were transferred to a series of three (3 × 3) (9-tube) modified Rappaport Vassiliadia broth tubes by loopful, respectively. After 24 h of subculture at 35 °C, turbid tubes were enumerated. The MPN index table was used for acquiring the MPN in test samples (Agriculture, 2014).
3. Discussion This study indicated that electron-beam irradiation at 2 kGy dose, after 10 days of treatment, is an efficient method to eliminate this pathogen. Two kGy in RTE intermediate-moisture foods of animal origin was determined using the optimum dose and the high performance of electron-beam irradiation to eliminate S. typhimurium (Cambero et al., 2012). Gamma irradiation at 3 kGy and modified atmosphere packaging (3% O2+ 50% CO2+ 47% N2) made safety of S. enteritidis and maintained qualities of meatballs (Gunes et al., 2011). Lactic acid of 5% was used as pre-treatment and 1 kGy irradiation dose of electron-beam to control Salmonella spp. in fresh beef meat (Li et al., 2015). 1% ginger extact besides using gamma irradiation were sufficient to keep the samples safe over 90 days but Salmonella spp. were not eliminated completely (Sediek et al., 2012). Gamma and electronbeam irradiation at 1.5 and 3 kGy on inoculated beef steaks eliminated S. typhimurium as well as reduced the total bacterial population (Chung et al., 2000).Electron-beam irradiation and refrigerated storage significantly decreased the total bacterial population. Kim et al. (2010) reported that the total bacterial population was decreased significantly with increasing irradiation dosage of beef jerky (Kim et al., 2010). The microbial population was decreased in 2–6 kGy dose of gamma irradiation in ground beef during refrigerated storage (Duong et al., 2008). Lopez- Gonzalez et al., (2000) reported the different sensory characteristics at 2 kGy of gamma and electron-beam radiation on beef patties, more sour flavors, salty, and sour tastes were determined in gamma irradiated samples (López-González et al., 2000). Cambero et al. (2012) demonstrated that 2 kGy dose of electron-beam irradiation maintains the organoleptic properties in RTE intermediate-moisture foods of animal origin.
1.5. Sensory evaluation Sensory evaluation was conducted with 10 trained consumers that were recruited based on their healthy health status and lack of allergyies. A presentation of tests was made with the use of a printed questionnaire read by the participants and an oral explanation was given to help our participants to fil our questionnaires. The participants' sense of color, odor, consistency, and taste were evaluated by using visual analogue scales (VAS, 0–10 cm). The standard scaling method is anchorded with like and dislike at the ends of the lines. The results are analyzed by converting the marks on lines into numbers (Svensson, 2012). Properties evaluation was performed on raw samples in the primary form, while the taste test was done only on the fried ones. The aim was to evaluate the participant's sensory acceptance of irradiated samples to determine the more suitable electron-beam dose needed to achieve microbiological safety with minimum or no effect on the acceptability. 1.6. Statistical analysis Statistical analyses were performed by SPSS Statistics 20. 2
Radiation Physics and Chemistry 168 (2020) 108524
F. Bouzarjomehri, et al.
Fig. 2. Effect of e-beam irradiation on the inoculated Salmonella typhimurium during refrigerated storage.
4. Conclusion
hamburgers, nuggets, and other meat products in different doses according to the sensory properties.
The results of this research showed the use of electron-beam irradiation at 0, 1, 2, 3 and 5 kGy doses not only reduced total bacterial population, but also eliminated Salmonella typhimurium. Two kGy dose of electron-beam irradiation was determined as an optimum dose with maintenance of 10 days of Salmonella typhimurium elimination and showed no undesirable effects on sensory characteristics. Therefore, applying the results of this study could be beneficial in meat industries in order to eliminate Salmonella Typhimurium and other pathogens. Further studies are required to determine the types of sausages,
Acknowledgements This present work has been supported financially by Reference Laboratory of Water and Wastewater, plant of electron-beam irradiation, Taft, Yazd, Iran. The authors are grateful to Dr. Milad BaradaranGhahfarokhi, Dr. Amin Salehi, and Dr. Mohammadhassan Dad for encouraging this project.
Fig. 3. Changes in sensory properties across the different doses (kGy) *Significant to control **Significant within groups. 3
Radiation Physics and Chemistry 168 (2020) 108524
F. Bouzarjomehri, et al.
Appendix A. Supplementary data
gamma irradiation with modified atmosphere packaging. J. Food Sci. 76, 413–420. Hwang, C.-A., Porto-Fett, A.C., Juneja, V.K., Ingham, S.C., Ingham, B.H., Luchansky, J.B., 2009. Modeling the survival of Escherichia coli O157: H7, Listeria monocytogenes, and Salmonella Typhimurium during fermentation, drying, and storage of soudjoukstyle fermented sausage. Int. J. Food Microbiol. 129, 244–252. Kim, H.-J., Chun, H.-H., Song, H.-J., Song, K.-B., 2010. Effects of electron beam irradiation on the microbial growth and quality of beef jerky during storage. Radiat. Phys. Chem. 79, 1165–1168. Leroy, F., Degreef, F., 2015. Convenient meat and meat products. Societal and technological issues. Appetite 94, 40–46. Li, S., Kundu, D., Holley, R.A., 2015. Use of lactic acid with electron beam irradiation for control of Escherichia coli O157: H7, non-O157 VTEC E. coli, and Salmonella serovars on fresh and frozen beef. Food Microbiol. 46, 34–39. Louis Coroller, A., Sabine Jeuge, B., Olivier Couvert, A., Souad Christieans, C., Mariem Ellouze, B., 2015. Extending the gamma concept to non-thermal inactivation: a dynamic model to predict the fate of Salmonella during the dried sausages process. Food Microbiol. 45, 266–275. Lung, H.-M., Cheng, Y.-C., Chang, Y.-H., Huang, H.-W., Yang, B.B., Wang, C.-Y., 2015. Microbial decontamination of food by electron beam irradiation. Trends Food Sci. Technol. 44, 66–78. Sachindra, N., Sakhare, P., Yashoda, K., Rao, D.N., 2005. Microbial profile of buffalo sausage during processing and storage. Food Control 16, 31–35. Sediek, L.E., Wafaa, A.M., Alkhalifah, D.H., Farag, S.E., 2012. Efficacy of ginger extract (Zingiber officinale) and gamma irradiation for quality and shelf-stability of processed frozen beef sausage. Life Sci. J. 9, 448–461. Svensson, L., 2012. Design and Performance of Small Scale Sensory Consumer Tests. Tahergorabi, R., Matak, K.E., Jaczynski, J., 2012. Application of electron beam to inactivate Salmonella in food: recent developments. Food Res. Int. 45, 685–694. Turner, C.W., 2010. Microbiology of ready‐to‐eat poultry products. Handb. Poult. Sci. Technol. 2, 507–515.
Supplementary data to this article can be found online at https:// doi.org/10.1016/j.radphyschem.2019.108524. References López‐González, V., Murano, P.S., Brennan, R.E., Murano, E.A., 2000. Sensory evaluation of ground beef patties irradiated by gamma rays versus electron beam under various packaging conditions. J. Food Qual. 23, 195–204. Agriculture, U.S.D.O., 2014. Most Probable Number Procedure and Tables: MLG Appendix 2.05. Laboratory Quality Assurance Staff (LQAS), pp. 1–8. Cambero, M.I., Cabeza, M.C., Escudero, R., Manzano, S., Garcia-Márquez, I., Velasco, R., Ordóñez, J.A., 2012. Sanitation of selected ready-to-eat intermediate-moisture foods of animal origin by E-beam irradiation. Foodborne Pathog. Dis. 9, 594–599. Chung, M.-S., Ko, Y.-T., Kim, W.-S., 2000. Survival of Pseudomonas fluorescens and Salmonella typhimurium after electron beam and gamma irradiation of refrigerated beef. J. Food Prot. 63, 162–166. Coburn, B., Grassl, G.A., Finlay, B., 2007. Salmonella, the host and disease: a brief review. Immunol. Cell Biol. 85, 112–118. Duong, D., Crandall, P., Pohlman, F., O’bryan, C., Balentine, C., Castillo, A., 2008. Improving ground beef safety and stabilizing color during irradiation using antioxidants, reductants or TSP. Meat Sci. 78, 359–368. Fallah, A.A., Saei-Dehkordi, S.S., Rahnama, M., 2010. Enhancement of microbial quality and inactivation of pathogenic bacteria by gamma irradiation of ready-to-cook Iranian barbecued chicken. Radiat. Phys. Chem. 79, 1073–1078. Gunes, G., Ozturk, A., Yilmaz, N., Ozcelik, B., 2011. Maintenance of safety and quality of refrigerated ready‐to‐cook seasoned ground beef product (meatball) by combining
4
Contents lists available at ScienceDirect
Radiation Physics and Chemistry journal homepage: www.elsevier.com/locate/radphyschem
The effect of electron-beam irradiation on microbiological properties and sensory characteristics of sausages
T
F. Bouzarjomehria, V. Dadb,c, B. Hajimohammadid, S.P. Shirmardie, A. Yousefi-Ghaleh Salimid,∗ a
Department of Medical Physics, Shahid Sadoughi University of Medical Sciences, Yazd, Iran Reference Laboratory of Water and Wastewater, Environment and Occupational Department, Shahid Sadoughi University of Medical Sciences, Yazd, Iran c Department of Microbiology, Kerman University of Medical Sciences, Kerman, Iran d Department of Food Safety and Hygiene, Faculty of Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran e Radiation Application Research School, Nuclear Science and Technology Research Institute (NSTRI), Tehran, Iran b
A R T I C LE I N FO
A B S T R A C T
Keywords: Electron treatment Salmonella typhimurium Beef sausages Sensory characteristics
The present study aimed to evaluate the survival of Salmonella typhimurium strain ATCC 14028, total bacterial populations and sensory characteristics of irradiated beef sausages. The samples were vacuum-packaged, irradiated by electron-beam, and stored in a refrigerator. Microbiological quality was promoted by irradiation dose increase. The effect of electron-beam on color, taste, odor and consistency characteristics showed no significant differences. The results indicated that using electron-beam irradiation at 2 kGy dose was a promising method in reducing bacterial populations, eliminating Salmonella typhimurium along with acceptability of sensory characteristics.
1. Introduction Nowadays, the request for ready-to-eat (RTE) and processed meat products have been increased due to their taste, convenience of use, low cost, and accessibility (Leroy and Degreef, 2015). Sausages are known as one of the most popular and delicious meats products worldwide (Sachindra et al., 2005). So far, over 2500 serotypes of Salmonella have been recognized. Approximately 2300 Salmonella strains cause salmonellosis, which is mainly characterized by abdominal pain, diarrhea, and nausea (Coburn et al., 2007). According to the Center for Disease Control (CDC) reports, among five pathogens that cause 90% of deaths, Salmonella accounts for 31% of it (Tahergorabi et al., 2012). CDC reported that 1.4 million salmonella illnesses occur annually in the U.S. which includes nearly 600 deaths and 16000 hospitalizations (Turner, 2010). The outbreaks of salmonellosis due to sausage consumption has been reported in England, Germany, France, Ireland, and the United States in 1995, 2001, 2008, 2011, 1997 and 2001, respectively (Louis Coroller et al., 2015). Electron-beam irradiation in the low-dose ionization radiation in the treatment of foods and crops could be applied for both industry and consumers interests due to eliminating microbial contamination (Lung et al., 2015). In comparison studies of electron beam irradiation on various attributes, it was effective to decrease total bacterial populations (Cambero et al., 2012) and Salmonella typhimurium (Hwang et al.,
∗
2009) in refrigerated beef. The majority of consumers are uncertain about the safety of sausages and have negative attitudes toward irradiated foods. Optimum dose irradiation with regards to sensory quality would be make the acceptance of irradiated hot dog smoked sausage. Despite high consumption with various ingredients, there is little information on the quality characteristics of irradiated hot dog smoked sausages. The objective of this study was to investigate This study aimed at evaluating the effectiveness of electron-beam irradiation in the treatment of contaminated sausages with Salmonella typhimurium, total bacterial population, and sensory characteristics. 1.1. Sample preparation and irradiation treatment The samples of hot dog smoked sausage (made from raw ground beef 70% (15% fat), with various ingredients such as starch 4.1%, ice 5%, sodium chloride 2%, sodium nitrite 0.3%, garlic 0.95%, ginger 0.95%, dextrose 0.7%, Paprika 0.5%, black pepper 0.5%) were ground for microbiological analysis. Sausages were divided into 25-g pieces and placed in vacuum bags. The vacuum-packaged sausages were packed in polyethylene box and transmitted to irradiation plant, exposed to electron-beam at the dose of 15 kGy before inoculating with Salmonella typhimurium (Fallah et al., 2010). The inoculated samples were achieved initial loads of approximately 108 C.F.U/g. The samples
Corresponding author. E-mail address: atefeh69yousefi@gmail.com (A. Yousefi-Ghaleh Salimi).
https://doi.org/10.1016/j.radphyschem.2019.108524 Received 11 November 2017; Received in revised form 30 August 2019; Accepted 10 October 2019 Available online 13 October 2019 0969-806X/ © 2019 Elsevier Ltd. All rights reserved.
Radiation Physics and Chemistry 168 (2020) 108524
F. Bouzarjomehri, et al.
were irradiated at doses of 0 (control), 1, 2, 3 and 5 kGy. The irradiated and non-irradiated samples were stored at 4 ± 0.5 °C in the refrigerator, excluding the ones which must be analyzed on day one. The samples were placed at room temperature for 50 min and analyzed for various days 0, 5, 10, 30 and 45. Fig. 1. Visual analogue scales (VAS).
1.2. Inoculum preparation
Independent sample T-test was used to determine differences at 95% confidence level.
All microbial cultures were prepared from the Merck company, Darmstadt, Germany. Salmonella enterica serotype Typhimurium ATCC 14028 was streaked onto nutrient agar, eosin methylene-blue lactose sucrose agar and mueller hinton agar and were incubated at 37 °C for 24 h. The colonies were transferred to selective enrichment broths (tryptic soy broth and nutrient broth) and incubated at 37 °C for 24 h. Then the incubated tubes (each with an equal volume) were centrifuged at 3000 g for 10 min at 20 °C. The obtained biomasses at the bottom of each tube were separated and transferred to 9 mL of buffered peptone water to acquire a population level of nearly 109 C.F.U/ml. One milliliter of the prepared suspension was transferred into irradiated (15 kGy) packages. Then, the samples were kneaded for 2 min and incubated at 35 °C for 24 h (Fallah et al., 2010).
2. Results 2.1. Microbiological properties The results for the survival of Salmonella typhimurium and total bacterial populations of beef sausages during storage at 4 °C (Fig. 1, Fig. 2). The microbiological quality of treated samples was significantly improved (p < 0.05). Salmonella typhimurium and total bacterial populations at doses of 2, 3, and 5 kGy to 3 log and at dose of 1 kGy to 0.3 and 2.2 log reduced, respectively.
1.3. Irradiation method 2.2. Sensory characteristics
Electron-beam irradiation was done in Central Processor Irradiation, Yazd, Iran. Electron-beam with 10 MeV was produced by rhodotron accelerator TT200 model (IBA, Belgium). One hundred samples in 25 gr pieces were moved at 5 m/s on a conveyor during of electron expose. Approximately, each sample was irradiated for 2 min. Doses of 0, 1, 2, 3 and 5 kGy were absorbed in each group. Dosimetry was conducted by FWT film (9F9, Goleta, CA). The absorption dose of each sample groups was: 1 ± %9, 2 ± %5, 3 ± %3, 5 ± %2.
The sensory characteristics of irradiated sausages showed no significant differences. The changes in VAS scores are represented in Fig. 3. Significant differences (to the control) in properties of color and odor (p < 0.05) were observed at 1 and 2 kGy doses, respectively. The results also indicated a significant difference (within groups) in the consistency of irradiated samples by 2 kGy dose (p < 0.05). There was a significant difference (within groups) of taste property at 0, 2 and 5 kGy doses.
1.4. Salmonella typhimurium enumeration Salmonella typhimurium was enumerated by the Most Probable Number (MPN), a method to approximate the population density of viable microorganisms. One gr of inoculated sausages were transferred to 10 mL of tetrathionate broth. These tubes were incubated at 35 °C for 24 h, and then 10, 1 and 0.1 mL of the enriched suspension were transferred to a series of three (3 × 3) (9-tube) modified Rappaport Vassiliadia broth tubes by loopful, respectively. After 24 h of subculture at 35 °C, turbid tubes were enumerated. The MPN index table was used for acquiring the MPN in test samples (Agriculture, 2014).
3. Discussion This study indicated that electron-beam irradiation at 2 kGy dose, after 10 days of treatment, is an efficient method to eliminate this pathogen. Two kGy in RTE intermediate-moisture foods of animal origin was determined using the optimum dose and the high performance of electron-beam irradiation to eliminate S. typhimurium (Cambero et al., 2012). Gamma irradiation at 3 kGy and modified atmosphere packaging (3% O2+ 50% CO2+ 47% N2) made safety of S. enteritidis and maintained qualities of meatballs (Gunes et al., 2011). Lactic acid of 5% was used as pre-treatment and 1 kGy irradiation dose of electron-beam to control Salmonella spp. in fresh beef meat (Li et al., 2015). 1% ginger extact besides using gamma irradiation were sufficient to keep the samples safe over 90 days but Salmonella spp. were not eliminated completely (Sediek et al., 2012). Gamma and electronbeam irradiation at 1.5 and 3 kGy on inoculated beef steaks eliminated S. typhimurium as well as reduced the total bacterial population (Chung et al., 2000).Electron-beam irradiation and refrigerated storage significantly decreased the total bacterial population. Kim et al. (2010) reported that the total bacterial population was decreased significantly with increasing irradiation dosage of beef jerky (Kim et al., 2010). The microbial population was decreased in 2–6 kGy dose of gamma irradiation in ground beef during refrigerated storage (Duong et al., 2008). Lopez- Gonzalez et al., (2000) reported the different sensory characteristics at 2 kGy of gamma and electron-beam radiation on beef patties, more sour flavors, salty, and sour tastes were determined in gamma irradiated samples (López-González et al., 2000). Cambero et al. (2012) demonstrated that 2 kGy dose of electron-beam irradiation maintains the organoleptic properties in RTE intermediate-moisture foods of animal origin.
1.5. Sensory evaluation Sensory evaluation was conducted with 10 trained consumers that were recruited based on their healthy health status and lack of allergyies. A presentation of tests was made with the use of a printed questionnaire read by the participants and an oral explanation was given to help our participants to fil our questionnaires. The participants' sense of color, odor, consistency, and taste were evaluated by using visual analogue scales (VAS, 0–10 cm). The standard scaling method is anchorded with like and dislike at the ends of the lines. The results are analyzed by converting the marks on lines into numbers (Svensson, 2012). Properties evaluation was performed on raw samples in the primary form, while the taste test was done only on the fried ones. The aim was to evaluate the participant's sensory acceptance of irradiated samples to determine the more suitable electron-beam dose needed to achieve microbiological safety with minimum or no effect on the acceptability. 1.6. Statistical analysis Statistical analyses were performed by SPSS Statistics 20. 2
Radiation Physics and Chemistry 168 (2020) 108524
F. Bouzarjomehri, et al.
Fig. 2. Effect of e-beam irradiation on the inoculated Salmonella typhimurium during refrigerated storage.
4. Conclusion
hamburgers, nuggets, and other meat products in different doses according to the sensory properties.
The results of this research showed the use of electron-beam irradiation at 0, 1, 2, 3 and 5 kGy doses not only reduced total bacterial population, but also eliminated Salmonella typhimurium. Two kGy dose of electron-beam irradiation was determined as an optimum dose with maintenance of 10 days of Salmonella typhimurium elimination and showed no undesirable effects on sensory characteristics. Therefore, applying the results of this study could be beneficial in meat industries in order to eliminate Salmonella Typhimurium and other pathogens. Further studies are required to determine the types of sausages,
Acknowledgements This present work has been supported financially by Reference Laboratory of Water and Wastewater, plant of electron-beam irradiation, Taft, Yazd, Iran. The authors are grateful to Dr. Milad BaradaranGhahfarokhi, Dr. Amin Salehi, and Dr. Mohammadhassan Dad for encouraging this project.
Fig. 3. Changes in sensory properties across the different doses (kGy) *Significant to control **Significant within groups. 3
Radiation Physics and Chemistry 168 (2020) 108524
F. Bouzarjomehri, et al.
Appendix A. Supplementary data
gamma irradiation with modified atmosphere packaging. J. Food Sci. 76, 413–420. Hwang, C.-A., Porto-Fett, A.C., Juneja, V.K., Ingham, S.C., Ingham, B.H., Luchansky, J.B., 2009. Modeling the survival of Escherichia coli O157: H7, Listeria monocytogenes, and Salmonella Typhimurium during fermentation, drying, and storage of soudjoukstyle fermented sausage. Int. J. Food Microbiol. 129, 244–252. Kim, H.-J., Chun, H.-H., Song, H.-J., Song, K.-B., 2010. Effects of electron beam irradiation on the microbial growth and quality of beef jerky during storage. Radiat. Phys. Chem. 79, 1165–1168. Leroy, F., Degreef, F., 2015. Convenient meat and meat products. Societal and technological issues. Appetite 94, 40–46. Li, S., Kundu, D., Holley, R.A., 2015. Use of lactic acid with electron beam irradiation for control of Escherichia coli O157: H7, non-O157 VTEC E. coli, and Salmonella serovars on fresh and frozen beef. Food Microbiol. 46, 34–39. Louis Coroller, A., Sabine Jeuge, B., Olivier Couvert, A., Souad Christieans, C., Mariem Ellouze, B., 2015. Extending the gamma concept to non-thermal inactivation: a dynamic model to predict the fate of Salmonella during the dried sausages process. Food Microbiol. 45, 266–275. Lung, H.-M., Cheng, Y.-C., Chang, Y.-H., Huang, H.-W., Yang, B.B., Wang, C.-Y., 2015. Microbial decontamination of food by electron beam irradiation. Trends Food Sci. Technol. 44, 66–78. Sachindra, N., Sakhare, P., Yashoda, K., Rao, D.N., 2005. Microbial profile of buffalo sausage during processing and storage. Food Control 16, 31–35. Sediek, L.E., Wafaa, A.M., Alkhalifah, D.H., Farag, S.E., 2012. Efficacy of ginger extract (Zingiber officinale) and gamma irradiation for quality and shelf-stability of processed frozen beef sausage. Life Sci. J. 9, 448–461. Svensson, L., 2012. Design and Performance of Small Scale Sensory Consumer Tests. Tahergorabi, R., Matak, K.E., Jaczynski, J., 2012. Application of electron beam to inactivate Salmonella in food: recent developments. Food Res. Int. 45, 685–694. Turner, C.W., 2010. Microbiology of ready‐to‐eat poultry products. Handb. Poult. Sci. Technol. 2, 507–515.
Supplementary data to this article can be found online at https:// doi.org/10.1016/j.radphyschem.2019.108524. References López‐González, V., Murano, P.S., Brennan, R.E., Murano, E.A., 2000. Sensory evaluation of ground beef patties irradiated by gamma rays versus electron beam under various packaging conditions. J. Food Qual. 23, 195–204. Agriculture, U.S.D.O., 2014. Most Probable Number Procedure and Tables: MLG Appendix 2.05. Laboratory Quality Assurance Staff (LQAS), pp. 1–8. Cambero, M.I., Cabeza, M.C., Escudero, R., Manzano, S., Garcia-Márquez, I., Velasco, R., Ordóñez, J.A., 2012. Sanitation of selected ready-to-eat intermediate-moisture foods of animal origin by E-beam irradiation. Foodborne Pathog. Dis. 9, 594–599. Chung, M.-S., Ko, Y.-T., Kim, W.-S., 2000. Survival of Pseudomonas fluorescens and Salmonella typhimurium after electron beam and gamma irradiation of refrigerated beef. J. Food Prot. 63, 162–166. Coburn, B., Grassl, G.A., Finlay, B., 2007. Salmonella, the host and disease: a brief review. Immunol. Cell Biol. 85, 112–118. Duong, D., Crandall, P., Pohlman, F., O’bryan, C., Balentine, C., Castillo, A., 2008. Improving ground beef safety and stabilizing color during irradiation using antioxidants, reductants or TSP. Meat Sci. 78, 359–368. Fallah, A.A., Saei-Dehkordi, S.S., Rahnama, M., 2010. Enhancement of microbial quality and inactivation of pathogenic bacteria by gamma irradiation of ready-to-cook Iranian barbecued chicken. Radiat. Phys. Chem. 79, 1073–1078. Gunes, G., Ozturk, A., Yilmaz, N., Ozcelik, B., 2011. Maintenance of safety and quality of refrigerated ready‐to‐cook seasoned ground beef product (meatball) by combining
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