Combined effects of aqueous chlorine dioxide and ultrasonic treatments on postharvest storage quality of plum fruit (Prunus salicina L.)

Postharvest Biology and Technology 61 (2011) 117–123

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Combined effects of aqueous chlorine dioxide and ultrasonic treatments on postharvest storage quality of plum fruit (Prunus salicina L.) Zhao Chen a , Chuanhe Zhu b,∗ a b

College of Life Sciences, Shandong Agricultural University, Daizong Street 61, Taian, Shandong 271018, PR China College of Food Science and Engineering, Shandong Agricultural University, Daizong Street 61, Taian, Shandong 271018,PR China

a r t i c l e

i n f o

Article history: Received 18 December 2010 Accepted 27 March 2011 Keywords: Chlorine dioxide Ultrasound Combined treatment Plum Postharvest Quality

a b s t r a c t The individual and combined effects of aqueous chlorine dioxide (40 mg L−1 ClO2 for 10 min) and ultrasonic (100 W ultrasound for 10 min) treatments on postharvest storage quality of plum fruit (Prunus salicina L.) were investigated. Two combination modes of these two treatments, treatment with ClO2 solution accompanied by simultaneous ultrasonic waves (one-step mode) and applying them sequentially (two-step mode) were adopted. The effect of combined treatments on maintaining contents of total flavonoids, ascorbic acid, reducing sugars, and titratable acids were similar but were more beneficial than the individual treatments and the untreated control. The one-step mode was more effective in reducing the initial microflora and retaining sensory qualities of plum fruit than the two-step mode, and fruit shelf-life could be extended to 60 d compared to 35 d for the control. Moreover, there were no detectable chemical residues in the treated samples with the one-step mode. These results demonstrated that the combined treatments of ClO2 and ultrasound could be a promising approach to maintain postharvest storage quality of plum fruit without significant risks to consumers. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Plums are highly perishable and storage duration is limited due to the occurrence of physiological disorders. Various chemical and physical methods have been undertaken to maintain postharvest plum fruit quality, including 1-methylcyclopropene, nitric oxide, calcium, cold storage, heat treatments, and controlled atmospheres (Serrano et al., 2004; Menniti et al., 2006; Larrigaudière et al., 2009; Luo et al., 2009; Singh et al., 2009). Chlorine dioxide (ClO2 ), a powerful sanitizer that has broad and high biocidal activity, is more stable and has a higher oxidizing capacity than chlorine. Unlike chlorine, ClO2 does not react with organic compounds to generate undesirable carcinogenic chemicals (Chen et al., 2010). This novel preservative, considered an alternative to chlorine in fruit and vegetable processing for its effectiveness and safety, therefore was used in this study on storage quality of plum fruit. ClO2 is legally permitted in China and USA for sanitizing fruit and vegetables in water (Ministry of Health of the People’s Republic of China, 2008; USFDA, 2010), though potable or clean water is still designated as the only decontamination agent for surface treatment of fresh produce in the European Union (EU, 2004).

∗ Corresponding author. Tel.: +86 538 8249157; fax: +86 538 8242850. E-mail address: [email protected] (C. Zhu). 0925-5214/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.postharvbio.2011.03.006

Ultrasonic technology is mainly applied in medical diagnostics, and industrial processes and inspections (Mizrach, 2008). Currently however, ultrasound has attracted considerable interest in food science and technology due to its promising applications in the food industry. It has been used in extraction of bioactive compounds (Rodrigues et al., 2008) and in microbial inactivation (Huang et al., 2006), although there is insufficient information about the effect of ultrasonic treatments on storage quality of fresh produce. Cao et al. (2010) recently reported that ultrasound was effective in inhibiting decay incidence and preserving quality in strawberries, but more evidence is needed to prove the effects of ultrasound on fruit and vegetables to promote the application of this technique. So far there have been no available reports studying the combined effects of ClO2 and ultrasonic treatments on storage quality of fruit and vegetables. The present research was therefore designed to investigate their combined effects on the postharvest quality of plum fruit.

2. Materials and methods 2.1. Plant material and preparation Plums (P. salicina L.) cv. ‘Black Diamond’ were harvested from a local orchard (Taian, China) at the commercial ripening stage. The fruit were transported to the laboratory and selected for uniformity

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of size (approx. 100 g) and color (purple black), with damaged fruit removed. 2.2. ClO2 and ultrasonic treatments In the first experiment, plums were treated with aqueous ClO2 at 20, 40, and 60 mg L−1 for 5, 10, and 15 min. A commercially available brand of stabilized ClO2 powder (Charmstar, Tianjin Charmstar Technology Development Co., Ltd., Tianjin, China) was dissolved in deionized water to prepare a stock solution (approx. 100 mg L−1 ) according to the manufacturer’s instructions. The concentration of ClO2 was measured by a standard method using iodimetry immediately before use (APHA, 1998). Then the stock solution was diluted with deionized water to prepare solutions with desired concentrations. Plums were subsequently washed with ClO2 solutions at different concentrations for different times with a ratio of 1 kg:5 L (fruit:ClO2 solution) at 20 ◦ C. Samples washed with potable tap water were used as controls to simulate commercial industrial processing. Following treatments, plums were rinsed in potable tap water for 1 min according to USFDA information (USFDA, 2010) and then air-dried. Control and ClO2 -treated samples were packaged into aseptic polyethylene bags (350 mm × 250 mm, 0.02 mm thick) and stored at 4 ◦ C for 60 d. Properties of the bags were specified by the manufacturer (Zhongda, Nanjing Zhongda Package Material Co., Nanjing, China) as follows: O2 permeability of 210–1615 mL m−2 h−1 MPa−1 ) (23 ◦ C, 0% RH) and CO2 permeability of 1060–8075 mL m−2 h−1 MPa−1 ) (23 ◦ C, 0% RH). The bags were not completely sealed as the aim was not to create a modified atmosphere environment, but to avoid moisture loss and mechanical damage of the fruit. In the second experiment, plums were subjected to ultrasonic waves of different strengths (80, 100, and 120 W) for different times (5, 10, and 15 min) at a constant frequency of 40 kHz. The experiments were carried out in an ultrasonic water bath (KQ3200DV, Kunshan Ultrasonic Instrument Co., Ltd., China; internal dimensions: 300 mm × 150 mm × 180 mm) with a ratio of 1 kg:5 L (fruit:water) at 20 ◦ C. Fruit treated by potable tap water were used as the control. The fruit were then removed from the bath, air-dried, and stored at 4 ◦ C for 60 d after being packaged. From the above two experiments, the ideal treatment conditions for reducing respiration rates and maintaining firmness were selected to carry out the third experiment. This experimental design was inspired by the work of Allende et al. (2007), who studied the impact of combined UV-C light, gaseous O3 , and modified atmosphere on postharvest strawberries. In their experiments, the effects of UV-C light and gaseous O3 on the respiration rate and overall visual quality were considered for the selection of the optimal doses, which were used for further research on the combined effects on more quality parameters. In the third experiment, the ideal treatments from the first two experiments were used to test and compare their combined effects with their individual application. Moreover, two combination modes of the ClO2 and ultrasonic treatment were utilized in order to evaluate synergistic effects between them. In the first combination mode (C1, one-step mode), plums were immersed into the ultrasonic chamber containing ClO2 solution at 20 ◦ C and subjected to simultaneous continuous ultrasound at 40 kHz. Our preliminary experiment indicated that ClO2 concentration was not affected by ultrasonic waves under the strength, frequency, and treatment time selected in this study for the combined treatment. In the second mode (C2, two-step mode), samples were treated firstly by ClO2 and then by ultrasound in a water bath at 20 ◦ C. Following ClO2 treatments in C1 and C2, samples were all rinsed with potable tap water for 1 min. After the combined treatments, fruit samples were air-dried, packaged, and stored at 4 ◦ C for 60 d. Fruit treated with potable tap water were used as controls.

In the third experiment, the ideal treatment conditions for maintaining contents of flavonoids, ascorbic acid, reducing sugars, and titratable acids were selected to perform the shelf-life study. Subsequently, the most effective treatment in prolonging the shelf-life was adopted to carry out further analysis. 2.3. Respiration rate Plums (approx. 500 g) were placed in a 3 L glass jar at 2 ◦ C and 95% RH. Humidified air flow was continuously pumped into the jars to avoid dehydration and excessive CO2 accumulation. Samples of 1 mL of headspace gas were taken from each glass jar and monitored using an infrared gas analyzer (GXH-1050, Beijing Junfang Chemical Institute of Technology, Beijing, China). The respiration rate was determined every 15 d for up to 60 d and expressed as mg kg−1 h−1 of CO2 production. 2.4. Firmness Firmness analysis was conducted every 15 d using a texture analyzer (TA-XT2i, Stable Micro Systems Ltd., Godalming, UK) with a 5 mm diameter cylindrical probe. Five fruit for each treatment were randomly selected and firmness was measured on the equatorial zone on two sides of each fruit, left and right side of the fruit suture. The penetration rate was 0.5 mm s−1 for a depth of 2 mm and results were expressed in N. 2.5. Contents of total flavonoids, ascorbic acid, reducing sugars, and titratable acids Nutrients were analyzed from the whole edible parts of plum fruit. The total flavonoid contents were determined every 15 d using a colorimetric method described by Kim et al. (2003). The results were expressed as mg of catechin equivalents per 100 g of plum fruit. The ascorbic acid, reducing sugars, and titratable acid contents of fruit were determined every 15 d according to Li et al. (2009). Ascorbic acid was titrated using the 2,6-dichloroindophenol titration method and its content was expressed as mg per 100 g of plum fruit. The content of reducing sugars was determined by the Fehling’s method and was calculated as g of glucose per 100 g of fruit. The content of titratable acids was obtained by titration with 0.1 mol L−1 sodium hydroxide to pH 8.2 and expressed as g of malic acid per 100 g of fruit. 2.6. Shelf-life Plums were stored at 4 ◦ C for 60 d for the shelf-life study. Samples washed with potable tap water were used as the controls. Fruit were taken for microbial growth assay and sensory quality evaluation on days 0, 35, 40, 55, and 60. Samples without treatment with potable tap water, ClO2 , or ultrasound were used to determine the inherent background microflora. The end of the shelf-life was defined as when the population of a microbial group reached an unacceptable level or the sensory quality evaluation panelists rejected the sample. To measure microbial levels, most of the external part of the fruit (30 g) was homogenized using a Stomacher 400 Circulator (Steward Ltd., London, UK) for 2 min in 270 mL of sterile neutralizing phosphate buffer. Ten-fold dilution series were made in 0.1% peptone water for plating. The following media and conditions were used for microbial incubation: Plate Count Agar was incubated at 30 ◦ C for 3 d for total aerobic mesophilic bacteria and also at 22 ◦ C for 5 d for total aerobic psychrotrophic bacteria; de Man–Rogosa–Sharpe medium (0.14% sorbic acid) was incubated at 30 ◦ C for 3 d for lactic acid bacteria; Rose Bengal Agar was incubated at 30 ◦ C for 3 d for yeasts and moulds. Colonies were counted and results

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expressed as log cfu g−1 . The following microbiological specifications were used to determine the end of the shelf-life: 8 log cfu g−1 for aerobic mesophilic bacteria and aerobic psychrotrophic bacteria, 7 log cfu g−1 (plus sensory analysis) for lactic acid bacteria, and 5 log cfu g−1 for yeasts and moulds (Gómez-López et al., 2008). Sensory quality was evaluated by a panel of six trained judges. Overall visual quality (OVQ) was scored based on a 9point hedonic scale (Chen et al., 2010): 9 = excellent, extremely fresh; 7 = very good, marketable; 5 = good, limit of marketability; 3 = fair, limit of usability; 1 = poor, unusable. The following sensory quality attributes were also evaluated according to GómezLópez et al. (2008): off-odors (1 = none, 3 = acceptable, 5 = severe); flavor (1 = fresh, 3 = acceptable, 5 = spoiled); texture (1 = fresh, 3 = acceptable, 5 = spoiled). The end of the shelf-life from the sensory quality point of view was reached when at least one of the mean scores was above the acceptability limit. 2.7. ClO2 , ClO2 − , and ClO3 − residues Fruit were manually peeled immediately after treatment. Both the external skin and the internal flesh were collected to test whether chemical residues existed on the fruit surface or within the fruit flesh. Samples were then homogenized with deionized water 5 times their weight for 30 s. The water extract was filtered through a 0.2 ␮m filter. The filtrate was collected to detect ClO2 , ClO2 − , and ClO3 − residues. The residual concentration of ClO2 was determined by the DPD (N,N-diethyl-p-phenylenediamine) method with a detection limit of 0.04 mg L−1 of filtrate (Trinetta et al., 2010). The byproducts of ClO2 , including ClO2 − and ClO3 − , were analyzed using an ion chromatography method (Tsai et al., 2001; Trinetta et al., 2010). The analytical column (IonPac AS9-SC, Dionex China Ltd., Beijing, China) was eluted with a 2 mmol L−1 Na2 CO3 /0.75 mmol L−1 NaHCO3 mobile phase at a flow rate of 2 mL min−1 . The detection limit was 0.01 mg L−1 of filtrate. The samples treated with potable tap water were used as the controls. The results were expressed as mg L−1 of filtrate and then converted to mg kg−1 of fruit. 2.8. Statistical analysis All assays were conducted in triplicate. Differences among samples were determined by least significant differences (LSD) using SigmaPlot 11.0 (Systat Software Inc., San Jose, CA, USA), and were considered to be significant when P < 0.05. 3. Results and discussion 3.1. Selection of ideal ClO2 and ultrasonic treatments Fruit respiration, a major factor contributing to postharvest quality losses, involves a series of oxidation-reduction reactions where various substances within the cells are oxidized to CO2 (Bhande et al., 2008). As the treatments with potable tap water for 5, 10, and 15 min were similar (P > 0.05), only the results of fruit treated for 15 min are shown. Based on the shelf-life study, the control samples became unacceptable from day 35. Thus, there was no need to determine all storage quality parameters on days 45 and 60. As shown in Fig. 1, the ClO2 and ultrasonic treatments obviously inhibited the respiratory response in the fruit. The respiration rates showed a typical climacteric pattern during ripening, similar to that described by several other authors (Serrano et al., 2004; Luo et al., 2009; Singh et al., 2009). The climacteric peak of the control was observed on day 15 while the ClO2 and the ultrasound treated fruit had a delayed climacteric peak on day 30, representing a 15 d lag, and produced lower level of CO2 production (P < 0.05). After reach-

Fig. 1. Respiration rate of plum fruit treated with (A) ClO2 and (B) ultrasound and stored for 60 d. Error bars represent the standard deviation.

ing the peak value, the respiration rates began to decrease in all samples until the end of storage. The respiration rate was more effectively inhibited by ClO2 than ultrasonic treatments. The level of CO2 production in the 20 mg L−1 ClO2 and the 80 W ultrasonic treated samples became lower as treatment times increased from 5 to 15 min. No significant differences between the samples treated with 40 and 60 mg L−1 ClO2 were observed and the 100 and 120 W ultrasonic treatments were also similar (P > 0.05). There were no differences between the 10 and 15 min treated samples by the 40 and 60 mg L−1 ClO2 , as well as by the 100 and 120 W ultrasound treatments (P > 0.05). Therefore, only the significant data are shown in Fig. 1 to simplify the data analysis. Our findings agreed with Zhong et al. (2006) who found that respiration rates of apricot were reduced and the maximum respiration rate delayed following the aqueous ClO2 treatment. However, López-Gálvez et al. (2010) reported that the respiration rate of fresh-cut lettuce was not influenced by aqueous ClO2 washing. These different results may be explained by different physiological features of experimental materials and different storage conditions. By applying ultrasound, Zhao et al. (2007) suppressed respiration rates of pears during ripening, in agreement with our work. Firmness change is one of the most important features of fruit ripening and senescence, largely reducing shelf-life, facilitating

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Fig. 3. Total flavonoids content of plum fruit treated with combined ClO2 and ultrasound and stored for 60 d. Error bars represent the standard deviation.

fruit, such as plums, the beginning of softening is associated with an increased respiration rate (Brummell and Harpster, 2001). Disassembly of the fruit cell wall may contribute to softening and textural changes during ripening. Furthermore, the process of softening is most likely driven by the energy provided by CO2 production, which could be a direct influence on the enzymatic breakdown of cell wall components (Hertog et al., 2004). Two ideal treatment conditions for reducing respiration rates and maintaining firmness were the 40 mg L−1 ClO2 treatment for 10 min and the 100 W ultrasonic treatment for 10 min, and so both were selected to study their individual and combined effects on chemical components. 3.2. Contents of total flavonoids, ascorbic acid, reducing sugars, and titratable acids Fig. 2. Firmness of plum fruit treated with (A) ClO2 and (B) ultrasound and stored for 60 d. Error bars represent the standard deviation.

pathogen infection, and limiting transportation (Luo et al., 2009). As shown in Fig. 2, a decrease in flesh firmness was observed during storage, irrespective of the treatment. Control fruit softened rapidly to about 15 N on day 30, which was a 57% decline. The ClO2 and ultrasound treated fruit showed a significantly higher flesh firmness than the untreated fruit (P < 0.05). The ClO2 treatments were relatively more effective in retaining firmness than the ultrasonic treatments. For the 20 mg L−1 ClO2 and the 80 W ultrasonic treatments, firmness became higher with increase in treatment time. There were no significant differences between the samples treated with 40 and 60 mg L−1 ClO2 and firmness of the samples treated with 100 and 120 W ultrasound were also similar (P > 0.05). For the 40 and 60 mg L−1 ClO2 and the 100 and 120 W ultrasonic treatments, the 10 and 15 min treatments were very similar (P > 0.05). Our results are in agreement with those of Zhong et al. (2006) and Niu et al. (2009), who found that aqueous ClO2 treatment could retain firmness of apricots and kiwifruit. Cao et al. (2010) have also reported that ultrasonic treatment significantly maintained higher levels of firmness in strawberry fruit during storage. The activities of ripening-related enzymes are largely responsible for fruit softening (Brummell and Harpster, 2001). The activities of these enzymes in plum fruit might be retarded by the ClO2 and ultrasonic treatments, and thus softening inhibited. In our research, fruit samples with lower respiration rates had lower firmness. In climacteric

There was a decrease in total flavonoids, ascorbic acid, and titratable acid contents in fruit during storage, while the reducing sugars contents increased gradually to maximum values on day 15 and decreased thereafter (Figs. 3–6). In the study of Díaz-Mula et al. (2009), increases in total phenolics was observed in plum fruit stored at 2 ◦ C for 35 d, which contrasted with our findings. However, Sun et al. (2001) reported that during a dual temperature cycle storage for 90 d (a cycle of −0.5 to 0 ◦ C for 15 d and 18 to 20 ◦ C for 1 d), phenolics in plum fruit decreased over time. They indicated that the decrease in phenolic contents in plum fruit was correlated with the increase in activity of polyphenol oxidase (PPO) and peroxidase (POD), oxidoreductases involved in phenolic oxidation. The results obtained by Manzocco et al. (1999) showed that PPO and POD activities increased from -30 to 20 ◦ C. In addition, Mirdehghan et al. (2007) found that low temperature storage increased total phenolic compounds in pomegranate arils. It is possible to speculate that lower temperatures may produce lower phenolic consumption rates. Hence, the differences among reports on the patterns of change of flavonoids in plum fruit may be attributed to different storage temperatures. Since the treatments with potable tap water for 10 min (control for C1) and 20 min (control for C2) were similar (P > 0.05), only the data of fruit treated for 20 min are shown. Higher levels of chemical components were observed in the C1 and C2 samples compared to the control, individual ClO2 and ultrasound treated samples (P < 0.05), while the differences between C1 and C2 were not significant (P > 0.05). From day 45, all contents in the

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Fig. 4. Ascorbic acid content of plum fruit treated with combined ClO2 and ultrasound and stored for 60 d. Error bars represent the standard deviation.

Fig. 6. Titratable acids content of plum fruit treated with combined ClO2 and ultrasound and stored for 60 d. Error bars represent the standard deviation.

ClO2 treated samples became higher than those in the ultrasound treated samples (P < 0.05). Similar results have been reported by Zhong et al. (2006) who found aqueous ClO2 treated apricots had higher titratable acidity and vitamin C contents compared with the controls through the postharvest period. Du et al. (2007) also maintained vitamin C contents in green bell peppers by using gaseous ClO2 treatments. However, some previous studies have indicated that ClO2 might have a negative effect on the contents of phenolic compounds and vitamin C (Vandekinderen et al., 2009). Since ClO2 as a strong oxidant can react with ascorbic acid and phenolics such as flavonoids (Gómez-López et al., 2009), it is possible that ClO2 may cause some detrimental effects on these compounds. One explanation for the reports on negative effects of ClO2 on nutrients could be due to the fact that fresh-cut products were selected as the experimental materials. Accordingly, ClO2 molecules might have more opportunities to penetrate into plant cells as a result of more direct exposure of flesh tissues, triggering the reaction with nutrients. Therefore, further research is needed to study why these differences exist

and how ClO2 acts upon chemical compounds of various fruit and vegetables. With respect to the ultrasonic treatment, in the work of Cao et al. (2010), the ultrasonic method was found to be effective in preserving titratable acidity and vitamin C contents in strawberries. Obviously, compared to their individual effects on chemical components of plum fruit, the effects of ClO2 and ultrasonic treatments were enhanced significantly by their combination (P < 0.05); however, treatment with ClO2 solution accompanied by simultaneous ultrasonic waves (C1) was not significantly different from applying them sequentially (C2) (P > 0.05). Therefore, these two combination modes were both adopted to conduct the following shelf-life study.

Fig. 5. Reducing sugars content of plum fruit treated with combined ClO2 and ultrasound and stored for 60 d. Error bars represent the standard deviation.

3.3. Shelf-life High loads of aerobic mesophilic (4.0 ± 0.4 log cfu g−1 ) and aerobic psychrotrophic bacteria (3.8 ± 0.5 log cfu g−1 ) were observed in the fresh plum fruit. Yeasts and moulds (3.0 ± 0.3 log cfu g−1 ) were present in relatively lower numbers, but lactic acid bacteria were not detected throughout storage period. As the treatments with potable tap water for 10 min (control for C1) and 20 min (control for C2) were similar (P > 0.05), only the results of fruit treated for 20 min are shown. Microbial counts decreased in the control, C1 and C2 samples immediately after treatments, whereas the combined treatments significantly reduced the microflora in plum fruit compared to the control (P < 0.05) (Table 1). Microorganisms showed a gradual growth during storage in all samples. The populations in the C1 and C2 samples were maintained at a lower level than those in the control (P < 0.05). The counts of aerobic mesophilic bacteria, aerobic psychrotrophic bacteria, yeasts and moulds in the control became unacceptable on day 40. However, the counts of C1 and C2 samples remained acceptable for 60 and 55 d, respectively. When the populations of aerobic mesophilic bacteria, aerobic psychrotrophic bacteria, yeasts and moulds were analyzed together, it can be concluded that, from the microbiological point of view, 25 and 20 d in shelf-life prolongation was achieved by the C1 and C2 treatments, respectively. Our previous study showed that an aqueous ClO2 treatment significantly reduced the initial microflora in fresh-cut asparagus lettuce and ClO2 treated samples had microflora populations at a lower level compared to the untreated control during storage (P < 0.05) (Chen et al., 2010). Kim et al. (2010) also found that aqueous ClO2 treat-

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Table 1 Microbial counts (log cfu g−1 ) of plum fruit treated with combined ClO2 and ultrasound and stored for 60 d. Microbial group

Treatment

Storage time (days) 0

Aerobic mesophilic bacteria

Aerobic psychrotrophic bacteria

Yeasts and moulds

Control C2 C1 Control C2 C1 Control C2 C1

35

3.9 1.6 0.9 3.7 1.5 0.8 2.7 1.3 0.7

± ± ± ± ± ± ± ± ±

0.4a 0.3b 0.2 0.2a 0.3b 0.2 0.3a 0.2b 0.2

7.3 3.9 3.0 7.5 3.8 2.9 4.2 2.7 2.0

± ± ± ± ± ± ± ± ±

0.3a 0.2b 0.4 0.4a 0.3b 0.3 0.4a 0.2b 0.3

40

55

60

8.5 ± 0.5a 5.6 ± 0.4b 4.8 ± 0.1 8.6 ± 0.4a 5.8 ± 0.3b 4.7 ± 0.5 5.5 ± 0.2a 3.5 ± 0.4b 2.6 ± 0.1

– 7.1 ± 0.3a 6.4 ± 0.2b – 7.3 ± 0.4a 6.1 ± 0.3b – 4.8 ± 0.3a 3.9 ± 0.4b

– 8.4 ± 0.5a 7.2 ± 0.5b – 8.3 ± 0.3a 7.3 ± 0.3b – 5.6 ± 0.4a 4.5 ± 0.4b

-, not determined. a Data are expressed as means±SD of triplicate assays. Numbers with underlines are counts above the acceptability limit. b Within the same microbial group, means with different letters in the same column are significantly different (P < 0.05) according to the LSD test.

ment significantly reduced the initial populations of total aerobic bacteria, yeasts and moulds in strawberries. Cao et al. (2010) found the increase in bacteria, yeast and mould growth was significantly inhibited by the ultrasonic treatment. Results of Huang et al. (2006) demonstrated that ultrasonication could enhance the bactericidal effect of ClO2 treatments on Salmonella and Escherichia coli O157:H7 inoculated on apples and lettuce. Scouten and Beuchat (2002) also reported that ultrasonic treatment had a modest enhancing effect on the effectiveness of Ca(OH)2 in killing or removing Salmonella and Escherichia coli O157:H7 inoculated on alfalfa seeds. However, they did not indicate whether any synergistic effects between chemical disinfectants and ultrasound existed as there was no comparison similar to C2 in our study on plum fruit. Our experimental design demonstrated that the ClO2 treatment with simultaneous ultrasonic waves synergistically improved their germicidal efficacies compared with using them sequentially, since C1 displayed obvious advantages over C2 in microbial decontamination (P < 0.05). One possible explanation for the synergistic disinfectant effects of chemical and ultrasonic treatments is that some microorganisms tightly attached to the fruit surface tissue may be difficult to be inactivated through a chemical approach. Through mechanical waves with high intensity, ultrasound can not only disrupt microbial cells but also facilitate the chemical decontamination process by dislodging these microorganisms, forcing them to be exposed directly to chemical disinfectants. As shown in Table 2, no significant differences in the same sensory quality attribute between the control and the treated samples were detected by the panelists immediately after treatment

(P > 0.05). Sensory quality declined in all samples as storage time prolonged. OVQ, off-odor, flavor, and texture of the controls were above the acceptability limit from day 40. The treated samples maintained higher sensory quality scores compared to the controls during storage (P < 0.05). The samples in C1 and C2 treatments were similar in the first 55 d (P > 0.05). OVQ and flavor of C2 samples became unacceptable on day 60. From the sensory quality point of view, a shelf-life prolongation of 25 and 20 d was achieved by the C1 and C2 treatments, respectively, which was consistent with the data of the microbial growth assay. Our previous work and that of other authors revealed that aqueous ClO2 treatment could maintain sensory quality of fruit and vegetables (Chen et al., 2010; Kim et al., 2010), while there is no adequate research on effects of ultrasound on sensory quality of fresh produce. 3.4. ClO2 , ClO2 − , and ClO3 − residues The most effective treatment in prolonging shelf-life was the C1 treatment, which was used to determine ClO2 , ClO2 − , and ClO3 − residues. The samples treated with potable tap water for 10 min were used as the control. In this study, no ClO2 , ClO2 − , or ClO3 − residues were detected in the skin or the flesh of the control and the C1 samples. As the skin and the flesh were all extracted with water 5 times their weight, ClO2 was less than 0.24 mg kg−1 while ClO2 − and ClO3 − were even less than 0.06 mg kg−1 . This result may attributed to the potable tap water rinse processing after treatment according to USFDA (2010), which was designed to remove any chemical residues on the fruit surface. Interestingly, Tsai et al. (2001) could not detect any residues of ClO2 − or ClO3 − on potato

Table 2 Sensory quality of plum fruit treated with combined ClO2 and ultrasound and stored for 60 d. Sensory quality attribute

Treatment

OVQ

Control C2 C1 Control C2 C1 Control C2 C1 Control C2 C1

Storage time (days) 0

Off-odor

Flavor

Texture

9.0 9.0 9.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0

35 ± ± ± ± ± ± ± ± ± ± ± ±

0.0a 0.0a 0.0a 0.0a 0.0a 0.0a 0.0a 0.0a 0.0a 0.0a 0.0a 0.0a

5.7 6.9 7.2 2.6 1.7 1.8 2.4 1.6 1.5 2.7 1.4 1.3

40 ± ± ± ± ± ± ± ± ± ± ± ±

0.3a 0.3b 0.4b 0.2a 0.3b 0.1b 0.4a 0.1b 0.3b 0.3a 0.5b 0.2b

4.3 6.6 6.5 4.6 2.2 2.1 5.0 2.3 2.4 5.0 1.9 2.0

± ± ± ± ± ± ± ± ± ± ± ±

0.5a 0.3b 0.5b 0.2a 0.3b 0.1b 0.3a 0.3b 0.2b 0.4a 0.1b 0.2b

55

60

– 5.7 ± 0.5a 6.0 ± 0.4a – 2.5 ± 0.2a 2.4 ± 0.3a – 2.7 ± 0.4a 2.6 ± 0.2a – 2.3 ± 0.2a 2.4 ± 0.3a

– 4.5 ± 0.3a 5.4 ± 0.3b – 2.7 ± 0.2a 2.8 ± 0.1a – 3.3 ± 0.2a 2.8 ± 0.1b – 2.6 ± 0.2a 2.6 ± 0.3a

–, Not determined. a Data are expressed as means ± SD of triplicate assays. Numbers with underlines are scores above the acceptability limit. b Within the same sensory quality attribute, means with different letters in the same column are significantly different (P < 0.05) according to the LSD test.

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surfaces stored in an atmosphere with ClO2 even if no rinse step was adopted. In the research of Trinetta et al. (2010), after the gaseous ClO2 treatment, the produce surfaces were immediately rinsed with water to remove any remaining ClO2 and byproducts. However, they found the use of ClO2 gas could still leave detectable residual levels on lettuce and sprout surfaces, while tomatoes, oranges, apples, strawberries, and cantaloupe had very low residues. Nonetheless, they concluded that products with these low levels would not likely to be harmful if consumed when compared to the USEPA acceptable levels for drinking water (maximum residual level for ClO2 at 0.8 mg L−1 and maximum contaminant level for ClO2 − at 1.0 mg L−1 ). In consideration of the importance of food safety to consumers, it is strongly recommended that treatments of fruit and vegetables with ClO2 should be followed by a potable water rinse. In summary, the combination of simultaneous ClO2 (40 mg L−1 ) and ultrasonic (100 W) treatments for 10 min maintained high storage quality of postharvest plum fruit during storage and prolonged the shelf-life for 25 d. This one-step mode has simplified the sanitizing procedure and may, to some extent, boost productivity. Nevertheless, it should be recognized that a treatment time of 10 min is relatively long for industrial practices and a shorter time would be more feasible. It is thus necessary to improve and optimize this technique to shorten the processing duration. In general, this novel application might be a promising method for practical commercial storage of plum fruit. Acknowledgements The authors are grateful to Dr. Zhenlin Han, Molecular Biosciences and Bioengineering Department, University of Hawaii, USA, for reviewing the manuscript. This research was financially supported by Department of Science & Technology of Shandong Province, PR China (2007BS06022). References Allende, A., Marín, A., Buendía, B., Tomás-Barberán, F., Gil, M., 2007. Impact of combined postharvest treatments (UV-C light, gaseous O3 , super atmospheric O2 and high CO2 ) on health promoting compounds and shelf-life of strawberries. Postharvest Biol. Technol. 46, 201–211. APHA (United States American Public Health Association), 1998. Standard Methods for the Examination of Water and Wastewater. American Public Health Association, Washington, DC. Bhande, S.D., Ravindra, M.R., Goswami, T.K., 2008. Respiration rate of banana fruit under aerobic conditions at different storage temperatures. J. Food Eng. 87, 116–123. Brummell, D.A., Harpster, M.H., 2001. Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol. Biol. 47, 311–340. Cao, S., Hu, Z., Pang, B., 2010. Optimization of postharvest ultrasonic treatment of strawberry fruit. Postharvest Biol. Technol. 55, 150–153. Chen, Z., Zhu, C., Zhang, Y., Niu, D., Du, J., 2010. Effects of aqueous chlorine dioxide treatment on enzymatic browning and shelf-life of fresh-cut asparagus lettuce (Lactuca sativa L.). Postharvest Biol. Technol. 58, 232–238. Díaz-Mula, H.M., Zapata, P.J., Guillén, F., Martínez-Romero, D., Castillo, S., Serrano, M., Valero, D., 2009. Changes in hydrophilic and lipophilic antioxidant activity and related bioactive compounds during postharvest storage of yellow and purple plum cultivars. Postharvest Biol. Technol. 51, 354–363. Du, J., Fu, M., Li, M., Xia, W., 2007. Effects of chlorine dioxide gas on postharvest physiology and storage quality of green bell pepper (Capsicum frutescens L. var longrum). Agric. Sci. China 6, 214–219. EU (European Union), 2004. Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of foodstuffs (including HACCP principles). Gómez-López, V.M., Ragaert, P., Jeyachchandran, V., Debevere, J., Devlieghere, F., 2008. Shelf-life of minimally processed lettuce and cabbage treated with gaseous chlorine dioxide and cysteine. Int. J. Food Microbiol. 121, 74–83.

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