Effects of Combined Treatments of Electron-Beam Irradiation and Addition of Leek ( Allium tuberosum ) Extract on Reduction of Pathogens in Pork Jerky

Abstract

This study investigated the combined effect of electron-beam irradiation and addition of leek (Allium tuberosum R.) extract on pork jerky inoculated with selected foodborne pathogens. Prepared pork jerky samples (control and samples with 1.0% leek extract) were inoculated with pathogens and subsequently irradiated at 0, 0.5, 1, 2, 3, and 4 kGy doses. In comparison with the control, samples with 1.0% leek extract showed significant reduction in the numbers of Escherichia coli, Listeria monocytogenes, and Salmonella Typhimurium. No viable counts were detected for Salmonella Typhimurium in both control and leek-extract samples, and for E. coli and L. monocytogenes in the leek-extract sample exposed to 3 kGy irradiation dose. The D₁₀ values for E. coli, L. monocytogenes, and Salmonella Typhimurium observed in the irradiated samples with leek extract were 0.39, 0.34, and 0.32 kGy, while the D₁₀ values in those without leek extract were 0.65, 0.65, and 0.39 kGy, respectively. Therefore, our results clearly showed that irradiation combined with leek extract was effective in reducing pathogens, suggesting that a low dose of irradiation combined with the addition of a natural antimicrobial agent can enhance the microbial safety and shelf-life of pork jerky.

Introduction

J erky is a typical dried food product that has become increasingly popular in many countries worldwide because it is nutritious and easy to carry. Dried foods have been known to have a stable shelf life (moisture to protein ratio, 0.75–1.00; a_w<0.70), and they can be stored at room temperature. However, the microbial safety of dried foods such as jerky is still being challenged, despite their low moisture content.

A number of reports have indicated that jerky may carry foodborne pathogens (Calicioglu et al., 2003; Kim et al., 2010; Yoon et al., 2005). Nummer et al. (2004) have reported that pathogenic microorganisms such as Escherichia coli O157, Listeria monocytogenes, and Salmonella spp. have been detected in jerky and were associated with outbreaks of foodborne illnesses. Outbreaks of E. coli O157:H7 and Salmonella occurred in the 1990s because of beef and venison jerky (Keene et al., 1997; CDC, 1995; USDA/FSIS, 2003). Levine et al. (2001) showed that foodborne pathogens such as L. monocytogenes and Salmonella spp. can survive the drying treatments in commercial jerky manufacturing, suggesting that effective protocols for the inactivation of these microorganisms are required.

Ionizing radiation is a non-thermal treatment used to enhance microbial food safety, and it has recently received substantial attention. In 1997, the U.S. Food and Drug Administration approved the use of irradiation for red meat. Commercial irradiators are generally divided into two types on the basis of the radiation source used: gamma rays and electron beams. The former type has a high penetrating power that can penetrate the product completely. Electron-beam irradiation has less influence on the quality of food because of its low penetrating power (Lewis et al., 2002), and it does not generate radioisotope concern (Black and Jaczynski, 2006), making the method more environmentally friendly and highly acceptable to consumers. Specifically, electron-beam irradiation can be applied to packaged foods (maximum thickness, 8 cm), thus reducing the chances of cross-contamination. Previous studies have shown that electron-beam irradiation significantly reduces microbial counts (Lewis et al., 2002; Song et al., 2009; Kim et al., 2010). Recently, x-ray-based irradiators that have some gamma and electron-beam irradiators have been developed and commercialized (Jeong et al., 2012).

A new trend in the processed food industry is to use a combined treatment that includes natural plant extracts (Lacroix et al., 2009b; Yun et al., 2010, 2011). Various botanical extracts from spices and herbs that contain antibacterial compounds and antioxidant have been used in combination with irradiation treatments (Oussalah et al., 2007). Ouattara et al. (2001) have demonstrated that these combined treatments effectively inhibited microorganisms at low doses of irradiation.

Species of the genus Allium are known for their antibacterial and antifungal properties (Rivlin, 2001; Griffiths et al., 2002). Leek, a member of Allium, has been used for treatment of abdominal pain, diarrhea, hematemesis, snakebite, and asthma (Zhong Yao Da Ci Dian, 1985). In a similar study, leek showed anti-carcinogenic effects on human cancer cells (Park et al., 2002), and recently, Yun et al. (2011) confirmed that leek extract combined with gamma irradiation was an efficient method for the inhibition of E. coli inoculated in pork.

The objective of this study was to investigate the synergistic effect of a combined treatment of electron-beam irradiation and leek extract on the survival of E. coli, L. monocytogenes, and Salmonella Typhimurium populations in pork jerky.

Materials and Methods

Sample preparation and sterilization

Pork loins and leeks were purchased from a local market in Daejeon, Korea. The pork loins were trimmed of all visible fat and subsequently sliced into 0.7-cm-thick pieces by using a meat slicer (model HFS 350G; Hankook Fugee Industries Co. Ltd., Seoul, Korea). The sliced pork samples were marinated at 4°C for 12 h. The marinade formula (w/w) used to prepare pork jerky is shown in Table 1.

Table 1.

Marinade Formula for the Pork Jerky

Ingredients	Amount (g/100 g meat)
Water	10
Soy sauce	9
Starch syrup	5
Sugar	2
d-Sorbitol	6
Ginger powder	0.1
Garlic powder	0.2
Onion powder	0.2
Potassium sorbate	0.1
leek extract	1.0 or none

Fresh leeks were washed with tap water and cut into approximately 10-cm pieces. The leek extract was obtained by treating leek with 70% ethyl alcohol for 72 h at room temperature, followed by evaporation of the solvent. The extract was then lyophilized (TFD5505; Ilshin Lab Co. Ltd., Seoul, Korea) to obtain a powder. Extraction with ethyl alcohol was the most effective method for antimicrobial effect among different preparation methods of leek extract (Yun et al., 2011).

Cured meat was sequentially dried using a dry oven (JSOF–150; JS Research Inc., Chungcheongnam-do, Korea) at 75°C, 65°C, and 55°C for 150, 90, and 60 min, respectively. After cooling, the jerky samples (A_w≈0.75) were packaged under aerobic condition. Before inoculation, the samples were randomly selected and sterilized using electron-beam irradiation (35 kGy at 2.5 MeV) with a linear electron beam RF accelerator (EB Tech, Daejeon, Korea).

Test pathogens and inoculation

E. coli (KCTC 1682), L. monocytogenes (KCTC 3569), and Salmonella Typhimurium (KCTC 1925) were obtained from the Korean Collection for Type Culture (KCTC, Daejeon, Korea). E. coli and L. monocytogenes were cultivated in tryptic soy broth (Difco Laboratories, Detroit, MI), and Salmonella Typhimurium was cultivated in nutrient broth (Difco Laboratories) at 37°C for 48 h. The cultures were then centrifuged (3,000×g for 10 min at 4°C) by using a refrigerated centrifuge (model VS-5500; Vision Scientific Co., Seoul, Korea). The resulting pellet was washed twice with sterile saline (0.85%) solution and suspended in the same saline solution. The viable cell density was approximately 10⁸ colony-forming units (CFU)/mL. The cut jerky samples (5 g, approximately 3.5 cm×3.5 cm) were inoculated with 100 μL of this solution. Each sample was then resealed and shaken for homogenization.

Electron-beam irradiation

Each inoculated sample (5 g) was irradiated on both sides by a linear electron beam RF accelerator (EB Tech). The energy level, beam power, and electric current used were 2.5 MeV, 40 kW, and 0–4.5 mA, respectively. Irradiation was performed in the presence of air with a conveyor velocity of 10 m/min and a dose rate of 1.1–4.4 kGy/s. Because of the low penetration power of the electron beam, all samples had a thickness of 1.0 cm to enhance the effectiveness of irradiation. To confirm the target dose, alanine dosimeters attached to the top and bottom surfaces of the sample pack were read using a 104 Electron Paramagnetic Resonance unit (model EMS-104; Bruker Instruments Inc., Billerica, MA). The maximum/minimum dose ratio was less than 1.004 for all samples. The doses used in this study were 0, 0.5, 1, 2, 3, and 4 kGy. The experiment was triplicated with two observation numbers at each replication. After irradiation, the samples were immediately stored under commercial storage conditions at 25°C, until required for further analysis.

Microbial analysis

Microbial analysis was done at the same day of irradiation. Each sample (5 g) was cut into small pieces (approximately 0.5 cm×0.5 cm) and homogenized for 2 min in a sterile stomacher bag containing 45 mL of sterile saline (0.85%) using a stomacher (bag mixer® 400; Interscience Co., St. Nom la Bretêche, France). Then, they were serially diluted in sterile saline (0.85%), and each diluent (0.1 mL) was spread on each bacterial media. Tryptic soy agar (Difco Laboratories) was used for E. coli and L. monocytogenes, whereas nutrient agar (Difco Laboratories) was used for Salmonella Typhimurium. The plates were incubated at 37°C for 48 h, and microbial counts were expressed as log CFU/g. Radiation sensitivity of the pathogens was calculated as D₁₀, a value that represents the dose required to inactivate 90% of the microbial population.

Statistical analysis

Statistical analysis was performed using one-way analysis of variance. When significant differences were detected, the differences among the mean values were identified using Duncan's multiple range tests with SAS software (SAS Institute, 2004) at a confidence level of p<0.05. Mean values and standard errors of the mean have been reported.

Results and Discussion

Effect of the combined treatment on E. coli is shown in Table 2. The initial populations of E. coli in the control and sample with leek extract were approximately 8.3 log CFU/g. With increasing irradiation doses, these populations continuously decreased in both samples (p≤0.05). In addition, the jerky with leek extract showed significantly lower (p≤0.05) E. coli populations at each irradiation dose than the samples not infused with the leek extract. Bacterial populations in the sample containing leek extract were below the detection limit (1 log CFU/g) after irradiation at 3 kGy.

Table 2.

Effect of Electron-Beam Irradiation on the Reduction of Escherichia coli (Log CFU/g) in Pork Jerky Without (Control) and With Added Leek Extract (1%)

	Pork jerky
Irradiation dose (kGy)	Control	Leek
0	8.34±0.02^a	8.30±0.04
0.5	6.41±0.05	5.75±0.04
1	4.50±0.01	3.94±0.08
2	3.78±0.05	2.42±0.09
3	2.98±0.04	ND^b
4	1.81±0.09	ND

Mean±standard deviation (n=4).

Viable with no growth at a detection limit<10¹ colony-forming units (CFU)/g.

The changes in the microbial populations of L. monocytogenes as a result of the treatments are shown in Table 3. Initial total viable counts for L. monocytogenes in the control and leek-extract pork jerky samples were approximately 8.3 log CFU/g. Addition of the leek extract significantly increased the radiosensitivity of L. monocytogenes, with no viable cell growth of the test microorganisms in the treated jerky and 2.43 log CFU/g in the control when treated at 3 kGy. This result confirmed that leek extract has a synergistic effect on the inhibition of the growth of L. monocytogenes in jerky.

Table 3.

Effect of Electron-Beam Irradiation on the Reduction of Listeria monocytogenes (Log CFU/g) in Pork Jerky Without (Control) and With Added Leek Extract (1%)

	Pork jerky
Irradiation dose (kGy)	Control	Leek
0	8.24±0.04^a	8.30±0.02
0.5	6.26±0.02	5.04±0.22
1	4.39±0.02	3.13±0.06
2	3.43±0.01	1.73±0.19
3	2.43±0.09	ND^b
4	1.72±0.17	ND

Mean±standard deviation (n=4).

Viable with no growth at a detection limit<10¹ colony-forming units (CFU)/g.

Table 4 shows the results for pork jerky samples inoculated with Salmonella Typhimurium. Here, we also detected a dose-dependent reduction in viable cell growth after irradiation treatments. Viable cells in the control samples were approximately 8.20 log CFU/g. However, irradiation at 3 kGy resulted in no detectable cell growth of the test pathogens in both samples.

Table 4.

Effect of Electron-Beam Irradiation on the Reduction of Salmonella Typhimurium (Log CFU/g) in Pork Jerky Without (Control) and With Added Leek Extract (1%)

	Pork jerky
Irradiation dose (kGy)	Control	Leek
0	8.19±0.02^a	8.22±0.03
0.5	6.45±0.03	6.31±0.02
1	5.62±0.06	5.40±0.15
2	3.49±0.16	2.44±0.09
3	ND^b	ND
4	ND	ND

Mean±standard deviation (n=4).

Viable with no growth at a detection limit<10¹ colony-forming units (CFU)/g.

S. Typhimurium was more sensitive to irradiation than E. coli and L. monocytogenes in the control samples at 3 and 4 kGy of irradiation doses. The number of Salmonella Typhimurium colonies in the samples exposed to 2-kGy irradiation reduced by approximately 4.70 and 5.78 log CFU/g in the control and leek-extract samples, respectively. This proved that incorporation of leek extracts in pork jerky was more effective in reducing Salmonella Typhimurium populations.

The results indicated that electron-beam irradiation at 3 kGy combined with leek extract treatment resulted in greater radiation-induced bacterial sterilization. The D ₁₀ values and relative radiation sensitivity (D₁₀ of sample with leek extract/D₁₀ of control; RRS) for different pathogens inoculated into pork jerky are presented in Table 5. Pork jerky treated with leek extract was more effective than the control samples at improving the radiation inactivation efficiency of all the tested microorganisms. The D ₁₀ value for E. coli in the control samples was 0.65 kGy and that in the treated samples was 0.39 kGy. Similarly, for L. monocytogenes, we obtained D ₁₀ values of 0.65 and 0.34 kGy for the control and treated samples, respectively, whereas, those for Salmonella Typhimurium were 0.39 and 0.32 kGy, respectively. Similarly, Jo et al. (2005) reported that D₁₀ value of Salmonella Typhimurium was shown to be considerably lower in seasoned and cooked beef compared to that of E. coli, Staphylococcus aureus, and L. ivanovii.

Table 5.

D ₁₀ Values (kGy) and Relative Radiation Sensitivity (RRS) for Different Pathogens Inoculated in Pork Jerky Without (Control) and With Added Leek Extract (1%)

Pathogens	Treatment	D₁₀ values (kGy)	RRS ^a
Escherichia coli	Control	0.65±0.01^b	1.000
	Leek	0.39±0.01	1.667
Listeria monocytogenes	Control	0.65±0.02	1.000
	Leek	0.34±0.01	1.912
Salmonella Typhimurium	Control	0.39±0.01	1.000
	Leek	0.32±0.01	1.219

Relative radiation sensitivity=D ₁₀ of control/D ₁₀ of the sample with added leek extract (1%).

Mean±standard deviation (I=4).

D₁₀ values for pathogenic bacteria in food are affected by water activity, food composition, irradiation or storage temperature, and presence of oxygen, among other factors (Mendonca, 2002). Cabeza et al. (2009) showed that D ₁₀ values for Listeria innocua, Salmonella Enteritidis, and Salmonella Typhimurium in dry fermented sausages ranged from 0.41 to 0.54 kGy. In addition, Sommers et al. (2003) demonstrated that bologna inoculated with L. monocytogenes showed a D ₁₀ value of 0.56 kGy after gamma irradiation, whereas the D ₁₀ value for the same pathogen in smoked salmon was 0.51 kGy after electron-beam irradiation (Medina et al., 2009).

The highest value of RRS (1.912) was observed for L. monocytogenes in the jerky treated with leek extract (Table 5). In recent studies, RRS values were considered when comparing the efficiency of irradiation under different treatment combinations (Lacroix et al., 2009a). Urbain (1986) has mentioned that various environmental factors affect the sensitivity of microorganisms to irradiation. Our results suggested that addition of leek extract provided an improved antimicrobial environment in pork jerky during irradiation and storage.

Extracts from plants are widely used in the food industry and are approved as Generally Recognized as Safe (Ahn et al., 2007). Plant extracts usually contain multiple compounds with antimicrobial activity attributed to a number of small terpenoid and phenolic compounds that, because of their lipophilic character, accumulate in bacterial membranes and induce energy depletion (Conner, 1993).

Recently, studies have been actively conducted on garlic (Allium sativum) and onion (Allium cepa), and there is an increased interest in the genus Allium. Leek is an Allium species known to have antioxidative properties because of a high amount of total polyphenol compounds and antimicrobial properties against several microorganisms (Ahn et al., 2005). Moon et al. (2003) reported that vitamin C and total phenol contents of leek are the major reason of its high antioxidative activiy.

In a previous study, leek showed strong antimicrobial effects on Pediococcus cerevisiae and Lactobacillus plantarum in Kimchi (Kim and Park, 1995). Moreover, Seo et al. (2001) demonstrated that leek showed antimicrobial activities against microorganisms present in food, such as E. coli O157:H7.

The results of the present study revealed that Gram-positive and Gram-negative bacteria were affected differently by the combination of electron-beam irradiation and leek extract. Salmonella Typhimurium (Gram-negative) was shown to be most sensitive to the treatment, as opposed to L. monocytogenes (Gram-positive) which showed the most resistance to the treatment. A study by Hao et al. (1998) showed that Gram-negative Aeromonas hydrophila was more sensitive to plant extracts and essential oils than Gram-positive L. monocytogenes. These differences are attributable to the structural differences of these bacteria (Davidson, 1997; Nikaido, 1996). Nikaido (1996) demonstrated that the cell wall of Gram-negative bacteria consists of lipopolysaccharides, which are hydrophilic, whereas the cell wall of Gram-positive bacteria mainly contains a thick layer of a unique peptidoglycan that is important for their survival.

Our results confirmed that a low dose of electron-beam irradiation was effective in inactivating foodborne pathogens in pork jerky. Furthermore, addition of leek improved the inactivation efficiency.

Conclusion

The present study showed that a low dose of electron-beam irradiation combined with the addition of leek extract can effectively enhance the microbial safety of jerky and reduce the hazards of foodborne pathogens.

Footnotes

Acknowledgments

This work was carried out with the support of Technology Development Program, Ministry for Food Agriculture, Forestry, and Fishery, Republic of Korea.

Disclosure Statement

No competing financial interests exist.

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