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Journal of Food Protection, Vol. 74, No. 6, 2011, Pages 899904 doi:10.4315/0362-028X.JFP-10-552
Copyright G, International Association for Food Protection

Inactivation of Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes in Orange and Tomato Juice Using Ohmic Heating
HUN-GU SAGONG,1 SANG-HYUN PARK,1 YOUNG-JIN CHOI,1 SANGRYEOL RYU,2
1Department

AND

DONG-HYUN KANG1*

of Food and Animal Biotechnology, School of Agricultural Biotechnology, Seoul National University, San 56-1, Sillim-dong, Kwanak-gu, Seoul 151-742, Korea; and 2Department of Food and Animal Biotechnology, Department of Agricultural Biotechnology, Center for Agricultural Biomaterials, and Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul 151-921, Korea MS 10-552: Received 14 December 2010/Accepted 27 January 2011

ABSTRACT
The effects of ohmic heating on reduction of Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes in orange and tomato juice were investigated. Orange and tomato juice inoculated with E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes were subjected to ohmic heating with selected parameters including electric field strength from 10 to 20 V/cm and treatment times from 0 to 540 s. The number of pathogens was reduced by increasing the electric field strength from 10 to 20 V/cm as well as increasing treatment time. The population of E. coli O157:H7 was reduced more than 5 log after 120, 210, and 540 s of treatment in orange juice with 20, 15, and 10 V/cm electric field strengths, respectively. In tomato juice, levels of E. coli O157:H7 were reduced more than 5 log after 90, 180, and 480 s with the same electric field strengths. Similar phenomena were observed for Salmonella Typhimurium and L. monocytogenes, but E. coli O157:H7 was the most resistant to ohmic heating treatment. These results show that ohmic heating is potentially useful for inactivation of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes and that the effect of inactivation depends on applied electric field strength, treatment time, pathogen species, and type of juice.

Escherichia coli O157:H7, Salmonella Typhimurium, and Listeria monocytogenes are important pathogens that can cause serious illnesses. E. coli O157:H7 is recognized as a major cause of diarrhea as well as hemolytic-uremic syndrome (11, 14, 17). The symptoms of infection caused by Salmonella spp. in humans include diarrhea, abdominal pain, mild fever, and chills (1). L. monocytogenes causes epidemic listeriosis (34). These pathogens have been associated with a wide range of foods, including ground fruit, vegetables, beef, raw milk, and contaminated water (3, 20, 23). Fruit and vegetable juices have also been reported as vehicles for outbreaks despite their low pH values (5, 6, 9, 15, 19). Therefore, these pathogens have become a major concern for the juice industry. The U.S. Food and Drug Administration (FDA) has finalized a hazard analysis and critical control point (HACCP) regulation that includes a performance criterion to assure juice safety (38); juice processors are required to implement a system that will achieve a minimum 5-log reduction of the most resistant organism in the juice being processed. Thermal processing is the most common method used to achieve a 5-log reduction of microorganisms in juice. Because conventional heating methods reduce nutritional and flavor qualities of juice and may produce undesirable off-flavor compounds (4, 21), the juice industry has been exploring alternative processing methods.
* Author for correspondence. Tel: 82-2-880-4927; Fax: 82-2-883-4928; E-mail: Kang7820@snu.ac.kr.

Ohmic heating is a promising technique for inactivation of foodborne pathogens and is widely used in blanching, evaporation, fermentation, gelation, and pasteurization of milk and in fruit juice processing (31, 33, 40). Ohmic heating occurs when an alternating electric current is passed through a food. The heat is internally generated due to electrical resistance of the food. Pathogens are therefore mainly destroyed via thermal inactivation (26, 27). The advantages of ohmic heating include rapid and uniform heating of food products. Therefore, the products obtained are of clearly superior quality with minimal structural, nutritional, or sensory changes and can be manufactured in a shorter operating time than with conventional heating (16, 30). Although considerable research on ohmic heating has been conducted during the last decade, to our knowledge there is no information on its use to inactivate E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes in fruit and vegetable juice. Thus, the aim of this study was to evaluate the efficacy of ohmic heating for inactivating E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes in orange and tomato juice with various exposure times and electric field strengths. MATERIALS AND METHODS
Bacterial strains. Strains of E. coli O157:H7 (ATCC 35150, ATCC 43889, ATCC 43890), Salmonella Typhimurium (ATCC 19586, ATCC 43174, DT 104), and L. monocytogenes (ATCC

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monocytogenes), and mixed before application of ohmic heating. The final cell concentration was 107 to 108 CFU/ml. Experimental set-up. We manufactured the laboratory-scale ohmic heater for this study (Fig. 1). The ohmic heating chamber consisted of a 2-liter Pyrex glass container of 0.5 cm thickness and two titanium plate electrodes. The electrode gap was 10 cm, and the cross-sectional area was 12 cm2. A K-type Teflon-coated thermocouple was used to measure the temperature in the treatment chamber. The supplied power in the chamber was alternating current at 60 Hz, and voltage was controlled by a variable transformer with a range of 100 to 200 V. The juice in the chamber was stirred with a magnetic stirrer during the ohmic heating treatment. Temperature, voltage, current, and time were recorded at 1-s intervals by a data logger (34790A, Agilent Technologies, Palo Alto, CA) and stored in a computer. Procedures for ohmic heat treatment. For the ohmic heating treatment, 200 ml of inoculated juice was placed in the 2liter ohmic chamber. The juice was stirred at medium speed to ensure uniform temperature. Three different electric field strengths (10, 15, and 20 V/cm) were applied to each fruit juice with various treatment times. The experiments were replicated three times. One milliliter of sample was withdrawn from the inoculated juices at 30- to 60-s intervals for up to 540 s during treatment and dispensed into test tubes containing 9 ml of sterile phosphate buffer (pH 7.0) in an ice-water bath. For enumeration of pathogens, 10-fold serial dilutions were prepared in sterile phosphate buffer, and 100 ml of sample or diluent was spread plated onto selective media (E. coli O157:H7, sorbitol MacConkey agar; Salmonella Typhimurium, xylose lysine desoxycholate agar; and L. monocytogenes, Oxford agar base with antimicrobic supplement Bacto [all Difco, BD]). All plates were incubated at 37uC for 24 to 48 h before counting. Statistical analysis. All experiments were duplicate plated and replicated three times. All data were analyzed with analysis of variance using Statistical Analysis System software (SAS Institute, Cary, NC) and Duncans multiple range test to determine if there were significant differences (P , 0.05) in mean values of microorganism populations.

FIGURE 1. Schematic diagram of the ohmic heating system.

7644, ATCC 19114, ATCC 19115) were obtained from the School of Food Science Bacterial Culture Collection, Washington State University, Pullman, for this study and used for all experiments. Stock cultures were prepared by combining 0.7 ml of a tryptic soy broth (TSB; Difco, BD, Sparks, MD) 24-h, 37uC culture with 0.3 ml of 50% glycerol and then stored at 280uC. Working cultures were streaked onto tryptic soy agar (TSA; Difco, BD), incubated at 37uC for 24 h, and stored at 4uC. Culture preparation. Each strain of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes was cultured in 5 ml of TSB at 37uC for 24 h, harvested by centrifugation at 4,000 | g for 20 min at 4uC, and washed three times with buffered peptone water (Difco, BD). The final pellets were resuspended in buffered peptone water, corresponding to approximately 108 to 109 CFU/ml. Mixed-culture cocktails were prepared by blending together equal volumes of each test strain. Sample preparation and inoculation. Different brands of pasteurized single-strength 100% orange juice (pH 3.72 and 11.8 uBrix) and tomato juice (pH 3.89 and 11.2 uBrix) without preservatives were purchased at a local supermarket (Seoul, Korea). Juice (200 ml, room temperature) was dispensed into a 2-liter ohmic chamber, inoculated with 10 ml of the mixed-culture cocktail (E. coli O157:H7, Salmonella Typhimurium, and L.

RESULTS The ohmic heating treatment times required for raising the temperatures of the orange and tomato juices from 28 to 80uC are given in Figure 2. The heating times decreased as a result of higher heating rates, resulting from the higher electric field strengths applied. As the electric field strengths

FIGURE 2. Ohmic heating curves of orange and tomato juice at different electric field strengths: tomato juice (%, 20 V/cm; ,, 15 V/cm; #, 10 V/cm) and orange juice (&, 20 V/cm; ., 15 V/cm; , 10 V/cm).

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increased, the heating rate of the juice increased. Tomato juice had higher heating rates than orange juice at all temperatures. Initial populations of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes in inoculated juices were approximately 107 to 108 CFU/ml, and the limit of detection was 1.0 log CFU/ml. Ohmic heating exhibited strong bactericidal activity against E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes. As electric field strength increased from 10 to 20 V/cm, surviving populations of the three pathogens decreased more effectively. Orange juice inoculated with the three pathogens was treated with electric field strengths of 10 to 20 V/cm. After 60, 90, 120, 150, 180, 210, 390, 420, 480, and 540 s of treatment with various electric field strengths, the surviving populations of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes were determined; results are shown in Figure 3. The levels of surviving cells of the three pathogens were reduced by $6 log to below the detection limit (1 log) within 120 s when treated with 20 V/cm electric field strength. However, when inoculated orange juice was treated with 15 and 10 V/cm electric field strengths, the reduction of each pathogen was generally decreased. At 15 V/cm electric field strength, levels of E. coli O157:H7 were significantly reduced by 4.67 log CFU/ml after 180 s compared with initial population; after 210 s treatment, they were below the detection limit. The populations of Salmonella Typhimurium experienced significant reductions of 1.8 log CFU/ml after 150 s and were below the detection limit after 180 s treatment. Populations of L. monocytogenes were reduced to 3.76 log CFU/ml after 180 s and below the detection limit after 210 s of treatment. At 10 V/cm electric field strength, populations of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes were reduced to below the detection limit after 540, 480, and 540 s of treatment, respectively. These results suggest that greater electric field strength increases the efficacy of ohmic heating in inoculated orange juice. Among the three pathogens, Salmonella Typhimurium was the most sensitive to ohmic heating in orange juice. Figure 4 shows surviving populations of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes in inoculated tomato juice treated with various electric field strengths from 20 to 10 V/cm. Ohmic heating with 20 V/cm electric field strength reduced the three pathogens to below the detection limit (1 log) after 90 s of treatment. At 15 V/cm electric field strength, E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes were reduced to below the detection limit after 180, 150, and 150 s of treatment, respectively; 10 V/cm electric field strength reduced these pathogens to below the detection limit after 480, 420, and 420 s of treatment, respectively. These results indicate that the bactericidal activity of ohmic heating in tomato juice is also proportional to electric field strength, as in the case of orange juice. However, the treatment time necessary to reduce pathogens to below the detection limit in tomato juice was less than that required for orange juice. Among the three pathogens, E. coli O157:H7 was more resistant to ohmic heating in tomato juice than were Salmonella Typhimurium and L. monocytogenes.

FIGURE 3. Survival curves for E. coli O157:H7 (a), Salmonella Typhimurium (b), and L. monocytogenes (c) in orange juice exposed to ohmic heating at 10 V/cm ( ), 15 V/cm (#), and 20 V/cm (.). The results are means from three experiments, and error bars indicate standard errors.

DISCUSSION Several studies have been conducted on the inactivation of foodborne pathogens in juice products using methods including pulsed electric field treatment (12), UV radiation (22), and high pressure (2). This study tested the inactivation of foodborne pathogens in orange and tomato juice by ohmic heating. The magnitude of reduction was influenced by treatment time, electric field strength, and kinds of pathogens and juices. All three pathogens were significantly reduced by ohmic heating treatment. The heat, which is internally generated in the treatment medium with rapidity and uniformity, is the major factor in bacterial inactivation (25, 26). However, many studies have demon-

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FIGURE 4. Survival curves for E. coli O157:H7 (a), Salmonella Typhimurium (b), and L. monocytogenes (c) in tomato juice exposed to ohmic heating at 10 V/cm ( ), 15 V/cm (#), and 20 V/cm (.). The results are means from three experiments, and error bars indicate standard errors.

strated that additional, nonthermal, effects of electricity contribute to microbial inactivation (7, 37). Chemicals, such as chloride-containing compounds (28) or hydrogen peroxide (35), produced in the treatment medium after low voltage alternating current treatment were found to cause bacterial death. Palaniappan et al. (26) and Shimada and Shimahara (36) reported membrane damage that caused permeability modification and leakage of cellular contents during mild electric field treatment. The combination of these factors may affect the inactivation of pathogens. The heat generation of ohmic heating is a function of the equation Q ~ kE2, where k is electrical conductivity and E is the electric field strength. From this equation, the heat generated is increased by increasing electrical conductivity

and electric field strength. Our results agree with the equation: more heat was generated as electric field strength increased. Due to rapid heat generation, the treatment time needed to achieve a 5-log reduction was decreased at the maximum electric field strength, and thus 20 V/cm electric field strength was the most effective treatment condition for inactivating the three pathogens in both orange and tomato juice. In addition, at 10 V/cm electric field strength, 540 s was required to achieve a minimum 5-log reduction of E. coli O157:H7 in orange juice, but only 120 s was required at 20 V/cm. In tomato juice, to achieve a minimum 5-log reduction of E. coli O157:H7, 480 s was required at 10 V/cm, but only 90 s was required at 20 V/cm electric field strength. Although the electric field was increased two times, the required treatment time to reduce a minimum 5-log reduction was substantially decreased, by almost 75%. Similar phenomena were observed for Salmonella Typhimurium and L. monocytogenes. The reason for these results is that the heat generated is in proportion to the square of the electric field strength. Thus, the required time for a minimum 5-log reduction of foodborne pathogens was dramatically reduced at 20 V/cm compared with 10 V/cm electric field strength. FDA HACCP rules mandate that fruit juice processors treat juice for a minimum 5-log reduction of the most resistant organism (38). Mazzotta (18) studied the thermal inactivation of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes in fruit juices. They observed that the D-values of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes at 60uC were 1.10, 0.21, and 0.43 min, respectively, in orange juice and that E. coli O157:H7 was the most resistant of the three pathogens. Based on our data, in both orange and tomato juices, more time was needed to reduce levels of E. coli O157:H7 to below the detection limit compared with Salmonella Typhimurium and L. monocytogenes. Thus, the ohmic heating pasteurization condition for these juices will be adapted to inactivation of E. coli O157:H7, the most resistant organism. Based on our results for ohmic heating treatment, a minimum 5-log reduction of E. coli O157:H7 in orange juice would require 120, 210, and 510 s treatment time at electric field strengths of 20, 15, and 10 V/cm, respectively; in tomato juice, 90, 180, and 480 s at electric field strengths of 20, 15, and 10 V/cm would be required. These results provide guidelines for establishing effective ohmic pasteurization conditions for the orange and tomato juice processing industries. In addition, the pH of orange juice (3.72) was lower than that of tomato juice (3.89), but treatment time to achieve a minimum 5-log reduction in tomato juice was from 30 to 60 s faster than in orange juice. The reason for this phenomenon may be that the electrical conductivity of tomato juice, due to salt added during processing (10, 13), was higher than that of orange juice at all temperatures. Therefore, the heating rate of tomato juice was higher than that of orange juice. Ruhlman et al. (32) reported that the electrical conductivity of tomato juice was higher than that of orange juice at all temperatures. Palaniappan and Sastry (24) also reported that heating rates in tomato juice were higher than in orange juice at all temperatures, due to the higher electrical conductivity of tomato juice.

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Although there has been no research on inactivation of E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes in fruit and vegetable juice by ohmic heating, other researchers have investigated the effects of ohmic heating on inactivation of other microorganisms. Cho et al. (8) found that survival curves and calculated D-values showed significantly higher lethality for Bacillus subtilis spores by ohmic heating than conventional heating. The efficacy of ohmic heating is primarily due to the thermal effect, but there is an additional killing effect caused by the electric current. Pereira et al. (29) studied death kinetics of E. coli in goats milk and Bacillus licheniformis in cloudberry jam treated by ohmic heating. In their study, lower D-values were obtained with ohmic treatment of E. coli in goats milk (D63uC ~ 1.9 min, D65uC ~ 0.86 min) compared with conventional treatment (D63uC ~ 3.9 min, D65uC ~ 3.5 min), and they observed similar effects on B. licheniformis in cloudberry jam. Yildiz and Baysal (39) reported that the numbers of Aspergillus niger were effectively reduced with an increase in electric field strength and temperature. A. niger was completely inactivated by alternating current heating at 36, 48, 68, and 108 V/cm for 30, 20, 12, and 6 s, respectively. In conclusion, the results of our study demonstrate that E. coli O157:H7, Salmonella Typhimurium, and L. monocytogenes in orange and tomato juice can be effectively inactivated by ohmic heating. The effect of inactivation depends on applied electric field strength, treatment time, pathogen species, and type of juice. However, for practical application by the juice industry, the efficacy of continuous ohmic heating as an intervention for the three pathogens must be further investigated. ACKNOWLEDGMENTS
This work was supported by grant R32-2008-000-10183-0 from the World Class University project of the Ministry of Education, Science & Technology and the Korea Science and Engineering Foundation through Seoul National University. This research was a part of the Technology Development Program for Agriculture (Agriculture Research Center program), supported by the Ministry for Food, Agriculture, Forestry and Fisheries, Republic of Korea.

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