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Effect of high oxygen atmospheres on fruit decay and quality in Chinese bayberries, strawberries and blueberries
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Food Control 19 (2008) 470–474 www.elsevier.com/locate/foodcont
Effect of high oxygen atmospheres on fruit decay and quality in Chinese bayberries, strawberries and blueberries Yonghua Zheng *, Zhenfeng Yang, Xuehong Chen College of Food Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, PR China Received 16 October 2006; received in revised form 19 May 2007; accepted 25 May 2007
Abstract The effects of high oxygen atmospheres on postharvest decay and quality of Chinese bayberry (Myrica rubra Seib & Zucc. cv. Wumei), strawberry (Fragaria ananassa Duch. cv. Fengxiang) and blueberry (Vaccinium corymbosum L. cv. Duke) fruit were assessed. Freshly harvested Chinese bayberries, strawberries and blueberries were placed in jars continuously ventilated with air or with 40%, 60%, 80% or 100% O2 at 5 °C for 9, 14 and 35 days. While the quality parameters of titratable acidity, total soluble solids and surface color measurements were only slightly affected by the superatmospheric O2 concentrations in all the three berries, treatments with 60–100% O2 significantly inhibited fruit decay. The severity of decay decreased with increasing O2 concentration. The 100% O2 treatment was the most effective in controlling fruit decay on all the three berries during storage at 5 °C. When the berries were removed from the high oxygen atmospheres and held for an additional 2 days in air at 20 °C, fruit treated with 60–100% O2 also exhibited significantly less decay rate, suggesting that high oxygen atmospheres had residual effect on decay control. The 40% O2 treatment was ineffective in controlling fruit decay on all the three berries. These data suggest that high oxygen atmospheres may provide a potential alternative for postharvest decay control on these berry fruit. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Chinese bayberry; Strawberry; Blueberry; High oxygen; Decay control; Quality parameters
1. Introduction With increasing consumer concern over pesticides residues on foods, along with pathogen resistance to many currently used pesticides, there is an urgent need to search for effective alternatives to control postharvest diseases of fruits and vegetables. Chinese bayberry, strawberry and blueberry are highly perishable soft fruit, susceptible to mechanical injury, physiological deterioration, water loss and microbiological decay. Grey mold rot, caused by Botrytis cinerea Pers.: Fr infection, is the most economically significant postharvest disease and the major factor in limiting shelf life on strawberry and blueberry fruit (Cappellini, Stretch, & Maiello, 1972; Garcia, Aguilera,
*
Corresponding author. Tel.: +86 25 84399080; fax: +86 25 84395618. E-mail address: [email protected] (Y. Zheng).
0956-7135/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2007.05.011
& Jimenez, 1996), while green mold rot is the major postharvest disease of Chinese bayberry (Qi, Wang, Liang, Zhou, & Cai, 2003). Effective control of fruit decay in fresh Chinese bayberry, strawberry and blueberry has been obtained by cold storage in combination with carbon dioxide-enriched atmospheres (10–20% CO2) (Ceponis & Cappelini, 1983, 1985; Gil, Holcroft, & Kader, 1997; Li & Kader, 1989; Shen & Huang, 2003). However, the higher CO2 concentrations necessary for decay control are often close to the level of product tolerance. Improper higher CO2 can initiate or aggravate physiological disorders, cause off-flavor and odors formation, and even increase decay susceptibility (Kader, 1995). High oxygen atmospheres (higher than 70% O2) have been suggested as a viable decay control alternative to pesticides for respiring products (Day, 1996). There have been many reports on the effects of high O2 atmospheres, alone or in combination with high CO2, on the in vitro growth of
Y. Zheng et al. / Food Control 19 (2008) 470–474
various pathogens associated with fresh fruits and vegetables (Amanatidou, Smid, & Gorris, 1999; Caldwell, 1965; Geysen et al., 2005; Robb, 1966) and on the in vivo microbial growth in fresh-cut vegetables (Allende, Jacxsens, Devlieghere, & Artes, 2003; Amanatidou, Slump, Gorris, & Smid, 2000; Jacxsens, Devlieghere, Van der Steen, & Debevere, 2001). In general, exposure to high O2 alone did not strongly inhibit microbial growth, while the combination of high O2 and high CO2 significantly suppressed microbial growth and prolonged shelf life of fresh-cut produce (Allende, Luo, McEvoy, Artes, & Wang, 2004; Amanatidou, Slump, & Smid, 2003). At present, relatively few studies have been conducted regarding the effects of high oxygen atmospheres on fruit decay control. The aim of this work was to investigate the effects of high O2 atmospheres on postharvest decay as well as on fruit quality for selected berry fruits: Chinese bayberry, strawberry and blueberry.
471
20 °C on a Bausch and Lomb refractometer. TA was determined by diluting each 5 mL aliquot of berry juice in 50 mL distilled water and then titrating to pH 8.2 using 0.1 N NaOH. 2.4. Surface color measurement External berry color was measured with a chromameter (CR 200, Minolta, Ramsey, NJ) which provided CIE L*, a* and b* values. These values were then used to calculate hue degree (h° = arctangent [b*/a*]), where 0° = red-purple; 90° = yellow; 180° = bluish-green; and 270° = blue. For Chinese bayberry and strawberry, two readings per fruit were taken on opposite cheeks of 10 fruits from each replicate. Since the stem end of blueberry fruit is the last to develop color (McGuire, 1992), blueberry fruit surface color was measured on this part using 10 fruits from each replicate. 2.5. Statistical analysis
2. Materials and methods 2.1. Fruits and treatments Chinese bayberry (Myrica rubra Seib & Zucc. cv. Wumei), strawberry (Fragaria ananassa Duch. cv. Fengxiang) and blueberry (Vaccinium corymbosum L. cv. Duke) were hand-harvested and sorted to eliminate damaged, shriveled and unriped fruit, and selected for uniform size and color. Three kilograms of Chinese bayberries and strawberries or 1.5 kg of blueberries were placed in each 18-l jar and three jars were used for each treatment. The jars were placed at 5 °C and linked by separate lines to continuous flow (120 ml/min) of humidified air (control), 40%, 60%, 80%, or 100% O2 (balanced with N2 in all high O2 treatments). All the gas atmospheres were humidified to approximately 90% RH by bubbling through water. The gases were checked regularly with an O2/CO2 analyzer (AMETEK, Pittsburgh, PA) and maintained at ±2% for the duration of the experiment. 2.2. Estimation of fruit decay Fruit decay was visually evaluated immediately after removal from the high O2 atmospheres at the end of storage and after an additional 1 or 2 days in air at 20 °C to simulate retail market conditions. Any berries with visible mold growth were considered decayed. Fruit decay was expressed as percentage of fruit showing decay symptoms. 2.3. Total soluble solids and total titratable acidity determinations At the end of storage, ten fruit of Chinese bayberry, strawberry and twenty fruit of blueberry from each replicate were wrapped in cheesecloth and squeezed with a hand press, and the juice was analyzed for total soluble solids (TSS), and titratable acidity (TA). TSS was determined at
ANOVA of data was performed for this experiment. Differences between means of data were compared by least significant difference (LSD) using Duncan’s multiple range test. Differences at P 6 0.05 were considered significant. 3. Results and discussion 3.1. Fruit decay Fruit decay in all the three berries was markedly affected by different high O2 concentrations. Chinese bayberries, strawberries and blueberries stored under air showed 21.1%, 27.7% and 40.3% fruit decay, respectively, at the end of storage at 5 °C. Treatment with 40% O2 had little effect on decay compared to fruit held in air in all three berries. Atmospheres enriched with O2 P 60% significantly inhibited Chinese bayberry, strawberry and blueberry fruit decay, and improved decay control was obtained with increased O2 concentration. 100% O2 was the most effective in suppressing fruit decay on all three berries among all treatments, with only 7.78%, 8.25% and 4.49% fruit decayed at the end of storage for Chinese bayberries, strawberries and blueberries, respectively (Tables 1–3). However, no significant difference was noted in Chinese bayberry and blueberry fruit decay between 80% O2 and 100% O2 treatments. The same pattern on fruit decay incidence was maintained after a subsequent 2 days holding period in air at 20 °C. Chinese bayberries, strawberries and blueberries that had been treated with 60–100% O2 exhibited significantly less decay after 1- and 2-day holding periods than those that had been stored in air or the 40% O2 atmospheres, suggesting that there are residual decay protection in 60–100% O2 treated fruits. In blueberries, 40% O2treatment even significantly promoted fruit decay during the subsequent 2 days holding period in air at 20 °C. High O2 atmospheres, alone or in combination with high CO2, have also been shown to inhibit fungal growth and decay
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Y. Zheng et al. / Food Control 19 (2008) 470–474
Table 1 Effect of high O2 atmospheres on Chinese bayberry fruit decay after 9 days of storage at 5 °C and after an additional 1 and 2 days in air at 20 °Ca Treatment
Decay (%) 9 days at 5 °C
Decay (%) 9 days at 5 °C plus 1 day in air at 20 °C
Decay (%) 9 days at 5 °C plus 2 days in air at 20 °C
Air 40% O2 60% O2 80% O2 100% O2
21.1a 22.2a 12.2b 8.89c 7.78c
43.9a 41.7a 28.5b 25.6b 16.8c
83.9a 82.7a 54.7b 51.9b 36.2c
a Data are expressed as mean of triplicate assays. Values in the same column having the same letter are not significantly different at p 6 0.05.
incidence in other studies. In strawberries, Wszelaki and Mitcham (2000) reported that there was a decrease in fruit decay with an increase in oxygen concentration above 40%. The 90% O2 and 100% O2 treatments had significantly less fruit decay than either the 15% CO2 itself or in combination with 40% O2 after 14 days of storage at 5 °C. Pe´rez and Sanz (2000) found that 100% O2 or 80% O2 in combination with 20% CO2 were more effective in controlling fungal decay than the conventional CA during storage at 8 °C. Fruit decay was also significantly reduced by high O2 modified atmosphere packaging (70% O2) compared with conventional MAP in strawberry and raspberry during storage at 7 °C (Van der Steen, Jacxsens, Devlieghere, & Debevere, 2002). However, the mechanisms by which high O2 atmospheres inhibit fruit decay are yet unclear. It is possible that atmospheres containing higher than 40% oxygen are toxic to decay microorganisms, due to the unfavorable effects of high oxygen on the oxidation–reduction potential of the system, the oxidation of certain enzymes especially those having sulfhydryl groups or disulfide bridges and the accumulation of injurious reactive oxygen species (Fridovitch, 1975). Wszelaki and
Mitcham (2000) found that 80–100% O2 was more effective in suppressing strawberry fruit decay caused by Botritis cinerea infection than in inhibiting the in vitro growth of Botritis cinerea itself, suggesting that the high oxygen atmospheres have an effect on the fruit itself as well as the decay fungus, thereby resulting in greater effect in vivo than in vitro. Modification of storage atmospheres has been shown to induce plant defensive responses and increase disease resistance in postharvest commodities. Carbon dioxide conditioning of avocado fruit before storage promoted levels of antifungal compounds (eg epitachin) and consequently delayed decay development by Colletotrichum gloeosporioides (Prusky, Plumbley, & Kobiler, 1991). Similarly, natural resistance of mango fruit to Alternaria alternata increased in response to carbon dioxide treatment (Prusky, Kobiler, Zauberman, & Fuchs, 1993). Therefore, whether the induced plant defensive responses also involve in the inhibitory effect of high oxygen atmosphere on fruit decay observed in this and other studies remains to be investigated. 3.2. TA and TSS After 9, 14 or 35 days of storage at 5 °C, TA content in Chinese bayberry, strawberry and blueberry fruit, respectively, was significantly lower than the initial value. No significant differences in TA content were observed among all of the high O2 and air treated fruit in all the three berries (Tables 4–6). However, Pe´rez and Sanz (2000) found significantly lower TA content in strawberry fruit exposed to 90% O2 + 10% CO2 than fruit held in air after 9 days of storage at 8 °C. TSS decreased during storage in all three berries. No significant differences were observed in TSS content among all of the high O2 treated and control fruit in Chinese bayberry (Table 4), while high O2 levels P60%
Table 2 Effect of high O2 atmospheres on strawberry fruit decay after 14 days of storage at 5 °C and after an additional 1 and 2 days in air at 20 °Ca Treatment
Decay (%) 14 days at 5 °C
Decay (%) 14 days at 5 °C plus 1 day in air at 20 °C
Decay (%) 14 days at 5 °C plus 2 days in air at 20 °C
Air 40% O2 60% O2 80% O2 100% O2
27.7a 25.1a 13.5b 11.2b 8.25c
53.9a 51.7a 29.1b 24.3b 17.4c
76.4a 72.7a 51.2b 49.9b 37.3c
a
Data are expressed as mean of triplicate assays.Values in the same column having the same letter are not significantly different at p 6 0.05.
Table 3 Effect of high O2 atmospheres on blueberry fruit decay after 35 days of storage at 5 °C and after an additional 1 and 2 days in air at 20 °Ca Treatment
Decay (%) 35 days at 5 °C
Decay (%) 35 days at 5 °C plus 1 day in air at 20 °C
Decay (%) 35 days at 5 °C plus 2 days in air at 20 °C
Air 40% O2 60% O2 80% O2 100% O2
40.3a 39.2a 19.5b 6.66c 4.49c
54.8b 62.7a 42.1c 22.9d 17.5d
67.5b 73.1a 47.7c 31.2d 25.4e
a
Data are expressed as mean of triplicate assays. Values in the same column having the same letter are not significantly different at p 6 0.05.
Y. Zheng et al. / Food Control 19 (2008) 470–474 Table 4 Effect of high O2 atmospheres on Chinese bayberry fruit quality during storage at 5 °Ca Day and treatment
TA (%)
TSS (%)
L*
Hue angle
Day 0 Day 9 air 40% O2 60% O2 80% O2 100% O2
0.77 0.66a 0.67a 0.67a 0.67a 0.68a
10.1 8.7a 8.9a 8.8a 8.9a 8.9a
22.1 22.4a 22.5a 23.6a 23.7a 23.1a
18.3 17.5a 17.2a 18.5a 18.8a 18.4a
a
Data are expressed as mean of triplicate assays for TA, TSS and of 30 assays for L* and Hue angle. Values in the same column having the same letter for day 9 are not significantly different at p 6 0.05.
Table 5 Effect of high O2 atmospheres on strawberry fruit quality during storage at 5 °Ca Day and treatment
TA (%)
TSS (%)
L*
Hue angle
Day 0 Day 14 air 40% O2 60% O2 80% O2 100% O2
0.76 0.66a 0.65a 0.66a 0.65a 0.67a
7.8 6.0b 5.8b 5.9b 6.3a 6.4a
42.7 43.2a 43.4a 43.9a 43.1a 42.8a
49.8 49.1a 49.1a 49.2a 48.4a 48.4a
a Data are expressed as mean of triplicate assays for TA, TSS and of 30 assays for L* and Hue angle. Values in the same column having the same letter for day 14 are not significantly different at p 6 0.05.
Table 6 Effect of high O2 atmospheres on blueberry fruit quality during storage at 5 °Ca Day and treatment
TA (%)
TSS (%)
L*
Hue angle
Day 0 Day 35 air 40% O2 60% O2 80% O2 100% O2
0.82 0.44a 0.41a 0.43a 0.44a 0.45a
11.0 8.5b 8.3b 9.0a 9.2a 9.5a
32.4 30.4a 30.5a 30.8a 30.5a 30.7a
5.72 308b 312b 334a 340a 341a
a Data are expressed as mean of triplicate assays for TA, TSS and of 30 assays for L* and Hue angle. Values in the same column having the same letter for day 35 are not significantly different at p 6 0.05.
tended to maintain higher TSS values than did 40% O2 and air in strawberry and blueberry fruit (Tables 5 and 6). After 14 days of storage at 5 °C, significantly higher values of TSS in 80% or 100% O2 treated strawberry fruit were detected in comparison with other high O2 and air treatments. After 35 days of storage at 5 °C, significantly higher values of TSS in three higher level O2 treated blueberry fruit were detected in comparison with 40% O2 and air treatments. However, no significant differences were observed in TSS between the two or among the three higher level O2 treatments in strawberry or blueberry fruit. On the contrary, significantly lower TSS values in high O2-treated strawberries than in air-stored fruit after storage at 5 °C were reported in earlier studies (Wszelaki & Mitcham, 2000; Pe´rez & Sanz, 2000). As the main substrates of respiratory metabolism, sugars and acids are depleted
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causing corresponding changes in TSS and TA during storage. It has been shown that exposure of harvested horticultural crops to superatmospheric O2 levels may stimulate, have no effect on, or reduce rates of respiration, depending on the commodity, maturity stage, time and temperature of storage, and O2,CO2 and ethylene concentrations (Kader & Ben-Yehoshua, 2000). The different change patterns of TA and TSS in different fruits and studies seem to be associated with the different effects of elevated O2 on commodity respiratory rate. 3.3. Fruit color Chinese bayberry and strawberry fruit surface color did not change significantly during storage. After 9 or 14 days of storage at 5 °C, comparable L and hue angle values were found among all of the high O2 treated and the air control fruit in both berries (Tables 4 and 5). Similarly, no significant differences were observed in fruit color of strawberries stored under high O2 atmospheres compared to air stored fruit (Pe´rez & Sanz, 2000; Wszelaki & Mitcham, 2000). On the contrary, there was a significant decrease in blueberry fruit surface L-value after 35 days of storage at 5 °C, indicating that the fruit became darker with storage. Comparable L-values were found among different high O2 treatment groups and the air control group (Table 6). The hue angle, which gives a better indication of blueberry color, increased during storage. Significantly higher hue angle values, indicating more blue color, were detected in fruits stored at 60–100% O2 than in other treatments after 35 days of storage. Different change patterns of fruit surface color in Chinese bayberries, strawberries and blueberries were perhaps due to the differences in composition and concentration of phenolic compounds. 4. Conclusion In summary, the data presented in this paper indicate that high O2 atmospheres significantly affect Chinese bayberry, strawberry and blueberry fruit decay during and after cold storage, whereas fruit quality was only mildly affected by high O2. High O2 concentrations between 60% and 100% generally had significantly less decay during cold storage at 5 °C and subsequent 2 days holding period in air at 20 °C. Acknowledgements This study was supported by the National Natural Science Foundation of China (No. 30170661). We thank Dr. Chien Yi Wang of Produce Quality and Safety Laboratory, Beltsville Agricultural Research Center, USDA, USA, to critically reading the manuscript. References Allende, A., Jacxsens, L., Devlieghere, F., & Artes, F. (2003). Microbial and sensory quality of fresh processed lettuce salad under high O2
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atmosphere throughout distribution chain. Acta Horticulturae, 600, 629–635. Allende, A., Luo, Y., McEvoy, J. L., Artes, F., & Wang, C. Y. (2004). Microbial and quality changes in minimally processed baby spinach leaves stored under superatmospheric oxygen and modified atmosphere conditions. Postharvest Biology and Technology, 33, 51–59. Amanatidou, A., Slump, R. A., Gorris, L. G. M., & Smid, E. J. (2000). High oxygen and high carbon dioxide modified atmospheres for shelflife extension of minimally processed carrots. Journal of Food Science, 65, 61–66. Amanatidou, A., Slump, R. A., & Smid, E. J. (2003). Microbial interactions on minimally processed carrots under elevated oxygen and carbon dioxide concentrations. Acta Horticulturae, 600, 621–628. Amanatidou, A., Smid, E. J., & Gorris, L. G. M. (1999). Effect of elevated oxygen and carbon dioxide on the surface growth of vegetable associated microorganisms. Journal of Applied Microbiology, 86, 429–438. Caldwell, J. (1965). Effects of high partial pressures of oxygen on fungi and bacteria. Nature, 206, 321–323. Cappellini, R. A., Stretch, A. W., & Maiello, J. M. (1972). Fungi association with blueberries held at various storage times and temperatures. Phytopathology, 62(1), 68–69. Ceponis, M. J., & Cappelini, R. A. (1983). Control of postharvest decays of blueberries by carbon dioxide-enriched atmospheres. Plant Disease, 67(2), 169–171. Ceponis, M. J., & Cappelini, R. A. (1985). Reducing decays in fresh blueberries with controlled atmospheres. HortScience, 20(2), 228–229. Day, B. P. F. (1996). High oxygen modified atmosphere packaging for fresh prepared produce. Postharvest News and Information, 7, 31N–34N. Fridovitch, I. (1975). Superoxide dismutase. Annual Review of Biochemistry, 44, 147–159. Garcia, J. M., Aguilera, C., & Jimenez, A. M. (1996). Gray mold in and quality of strawberry fruit following postharvest heat treatment. HortScience, 31(2), 255–257. Geysen, S., Geeraerd, A. H., Verlinden, B. E., Michiels, C. W., Van Impe, J. F., & Nicolaı¨, B. M. (2005). Predictive modelling and validation of Pseudomonas fluorescence growth at superatmospheric oxygen and carbon dioxide concentrations. Food Microbiology, 22, 149–158. Gil, M. I., Holcroft, D. M., & Kader, A. A. (1997). Changes in strawberry anthocyanins and other polyphenols in response to carbon dioxide
treatments. Journal of Agricultural and Food Chemistry, 45(5), 1662–1667. Jacxsens, L., Devlieghere, F., Van der Steen, C., & Debevere, J. (2001). Effect of high oxygen modified atmosphere packaging on microbial growth and sensorial qualities of fresh-cut produce. International Journal of Food Microbiology, 71, 197–210. Kader, A. A. (1995). Regulation of fruit physiology by controlled/ modified atmospheres. Acta Horticulturae, 398, 59–70. Kader, A. A., & Ben-Yehoshua, S. (2000). Effects of superatmospheric oxygen levels on postharvest physiology and quality of fresh fruits and vegetables. Postharvest Biology and Technology, 20, 1–13. Li, C., & Kader, A. A. (1989). Residual effects of controlled atmospheres on postharvest physiology and quality of strawberries. Journal of American Society for Horticultural Sciences, 114, 405–407. McGuire, R. G. (1992). Reporting of objective color measurements. HortScience, 27, 1254–1255. Pe´rez, A. G., & Sanz, C. (2000). Effect of high-oxygen and high-carbondioxide atmospheres on strawberry flavor and other quality traits. Journal of Agricultural and Food Chemistry, 49, 2370–2375. Prusky, D., Kobiler, H., Zauberman, G., & Fuchs, Y. (1993). Preharvest conditions and postharvest treatments affecting the incidence of decay in mango fruits during storage. Acta Horticulturae, 341, 305–320. Prusky, D., Plumbley, R. A., & Kobiler, H. (1991). Modulation of natural resistance of avocado fruits to Colletotrichium gloesporiodes by CO2 treatment. Physiological and Molecular Plant Pathology, 39, 325–334. Qi, X. J., Wang, L. P., Liang, S. M., Zhou, L. Q., & Cai, X. Q. (2003). Study on the mycoflora in bayberry (Myrica rubra) fruits treated by controlled atmosphere storage. Acta Agriculturae Zhejianggens, 15(1), 28–30. Robb, S. M. (1966). Reactions of fungi to exposure to 10 atmospheres pressure oxygen. Journal of General Microbiology, 45, 17–29. Shen, L. Q., & Huang, G. R. (2003). Study on modified atmosphere packaging of Myrica rubra. Journal of Zhejiang University of Science and Technology, 15, 232–235. Van der Steen, C., Jacxsens, L., Devlieghere, F., & Debevere, J. (2002). Combining high oxygen atmospheres with low oxygen modified atmosphere packaging to improve the keeping quality of strawberries and raspberries. Postharvest Biology and Technology, 26, 49–58. Wszelaki, A. L., & Mitcham, E. J. (2000). Effects of superatmospheric oxygen on strawberry fruit quality and decay. Postharvest Biology and Technology, 20, 125–133.
Food Control 19 (2008) 470–474 www.elsevier.com/locate/foodcont
Effect of high oxygen atmospheres on fruit decay and quality in Chinese bayberries, strawberries and blueberries Yonghua Zheng *, Zhenfeng Yang, Xuehong Chen College of Food Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, PR China Received 16 October 2006; received in revised form 19 May 2007; accepted 25 May 2007
Abstract The effects of high oxygen atmospheres on postharvest decay and quality of Chinese bayberry (Myrica rubra Seib & Zucc. cv. Wumei), strawberry (Fragaria ananassa Duch. cv. Fengxiang) and blueberry (Vaccinium corymbosum L. cv. Duke) fruit were assessed. Freshly harvested Chinese bayberries, strawberries and blueberries were placed in jars continuously ventilated with air or with 40%, 60%, 80% or 100% O2 at 5 °C for 9, 14 and 35 days. While the quality parameters of titratable acidity, total soluble solids and surface color measurements were only slightly affected by the superatmospheric O2 concentrations in all the three berries, treatments with 60–100% O2 significantly inhibited fruit decay. The severity of decay decreased with increasing O2 concentration. The 100% O2 treatment was the most effective in controlling fruit decay on all the three berries during storage at 5 °C. When the berries were removed from the high oxygen atmospheres and held for an additional 2 days in air at 20 °C, fruit treated with 60–100% O2 also exhibited significantly less decay rate, suggesting that high oxygen atmospheres had residual effect on decay control. The 40% O2 treatment was ineffective in controlling fruit decay on all the three berries. These data suggest that high oxygen atmospheres may provide a potential alternative for postharvest decay control on these berry fruit. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Chinese bayberry; Strawberry; Blueberry; High oxygen; Decay control; Quality parameters
1. Introduction With increasing consumer concern over pesticides residues on foods, along with pathogen resistance to many currently used pesticides, there is an urgent need to search for effective alternatives to control postharvest diseases of fruits and vegetables. Chinese bayberry, strawberry and blueberry are highly perishable soft fruit, susceptible to mechanical injury, physiological deterioration, water loss and microbiological decay. Grey mold rot, caused by Botrytis cinerea Pers.: Fr infection, is the most economically significant postharvest disease and the major factor in limiting shelf life on strawberry and blueberry fruit (Cappellini, Stretch, & Maiello, 1972; Garcia, Aguilera,
*
Corresponding author. Tel.: +86 25 84399080; fax: +86 25 84395618. E-mail address: [email protected] (Y. Zheng).
0956-7135/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2007.05.011
& Jimenez, 1996), while green mold rot is the major postharvest disease of Chinese bayberry (Qi, Wang, Liang, Zhou, & Cai, 2003). Effective control of fruit decay in fresh Chinese bayberry, strawberry and blueberry has been obtained by cold storage in combination with carbon dioxide-enriched atmospheres (10–20% CO2) (Ceponis & Cappelini, 1983, 1985; Gil, Holcroft, & Kader, 1997; Li & Kader, 1989; Shen & Huang, 2003). However, the higher CO2 concentrations necessary for decay control are often close to the level of product tolerance. Improper higher CO2 can initiate or aggravate physiological disorders, cause off-flavor and odors formation, and even increase decay susceptibility (Kader, 1995). High oxygen atmospheres (higher than 70% O2) have been suggested as a viable decay control alternative to pesticides for respiring products (Day, 1996). There have been many reports on the effects of high O2 atmospheres, alone or in combination with high CO2, on the in vitro growth of
Y. Zheng et al. / Food Control 19 (2008) 470–474
various pathogens associated with fresh fruits and vegetables (Amanatidou, Smid, & Gorris, 1999; Caldwell, 1965; Geysen et al., 2005; Robb, 1966) and on the in vivo microbial growth in fresh-cut vegetables (Allende, Jacxsens, Devlieghere, & Artes, 2003; Amanatidou, Slump, Gorris, & Smid, 2000; Jacxsens, Devlieghere, Van der Steen, & Debevere, 2001). In general, exposure to high O2 alone did not strongly inhibit microbial growth, while the combination of high O2 and high CO2 significantly suppressed microbial growth and prolonged shelf life of fresh-cut produce (Allende, Luo, McEvoy, Artes, & Wang, 2004; Amanatidou, Slump, & Smid, 2003). At present, relatively few studies have been conducted regarding the effects of high oxygen atmospheres on fruit decay control. The aim of this work was to investigate the effects of high O2 atmospheres on postharvest decay as well as on fruit quality for selected berry fruits: Chinese bayberry, strawberry and blueberry.
471
20 °C on a Bausch and Lomb refractometer. TA was determined by diluting each 5 mL aliquot of berry juice in 50 mL distilled water and then titrating to pH 8.2 using 0.1 N NaOH. 2.4. Surface color measurement External berry color was measured with a chromameter (CR 200, Minolta, Ramsey, NJ) which provided CIE L*, a* and b* values. These values were then used to calculate hue degree (h° = arctangent [b*/a*]), where 0° = red-purple; 90° = yellow; 180° = bluish-green; and 270° = blue. For Chinese bayberry and strawberry, two readings per fruit were taken on opposite cheeks of 10 fruits from each replicate. Since the stem end of blueberry fruit is the last to develop color (McGuire, 1992), blueberry fruit surface color was measured on this part using 10 fruits from each replicate. 2.5. Statistical analysis
2. Materials and methods 2.1. Fruits and treatments Chinese bayberry (Myrica rubra Seib & Zucc. cv. Wumei), strawberry (Fragaria ananassa Duch. cv. Fengxiang) and blueberry (Vaccinium corymbosum L. cv. Duke) were hand-harvested and sorted to eliminate damaged, shriveled and unriped fruit, and selected for uniform size and color. Three kilograms of Chinese bayberries and strawberries or 1.5 kg of blueberries were placed in each 18-l jar and three jars were used for each treatment. The jars were placed at 5 °C and linked by separate lines to continuous flow (120 ml/min) of humidified air (control), 40%, 60%, 80%, or 100% O2 (balanced with N2 in all high O2 treatments). All the gas atmospheres were humidified to approximately 90% RH by bubbling through water. The gases were checked regularly with an O2/CO2 analyzer (AMETEK, Pittsburgh, PA) and maintained at ±2% for the duration of the experiment. 2.2. Estimation of fruit decay Fruit decay was visually evaluated immediately after removal from the high O2 atmospheres at the end of storage and after an additional 1 or 2 days in air at 20 °C to simulate retail market conditions. Any berries with visible mold growth were considered decayed. Fruit decay was expressed as percentage of fruit showing decay symptoms. 2.3. Total soluble solids and total titratable acidity determinations At the end of storage, ten fruit of Chinese bayberry, strawberry and twenty fruit of blueberry from each replicate were wrapped in cheesecloth and squeezed with a hand press, and the juice was analyzed for total soluble solids (TSS), and titratable acidity (TA). TSS was determined at
ANOVA of data was performed for this experiment. Differences between means of data were compared by least significant difference (LSD) using Duncan’s multiple range test. Differences at P 6 0.05 were considered significant. 3. Results and discussion 3.1. Fruit decay Fruit decay in all the three berries was markedly affected by different high O2 concentrations. Chinese bayberries, strawberries and blueberries stored under air showed 21.1%, 27.7% and 40.3% fruit decay, respectively, at the end of storage at 5 °C. Treatment with 40% O2 had little effect on decay compared to fruit held in air in all three berries. Atmospheres enriched with O2 P 60% significantly inhibited Chinese bayberry, strawberry and blueberry fruit decay, and improved decay control was obtained with increased O2 concentration. 100% O2 was the most effective in suppressing fruit decay on all three berries among all treatments, with only 7.78%, 8.25% and 4.49% fruit decayed at the end of storage for Chinese bayberries, strawberries and blueberries, respectively (Tables 1–3). However, no significant difference was noted in Chinese bayberry and blueberry fruit decay between 80% O2 and 100% O2 treatments. The same pattern on fruit decay incidence was maintained after a subsequent 2 days holding period in air at 20 °C. Chinese bayberries, strawberries and blueberries that had been treated with 60–100% O2 exhibited significantly less decay after 1- and 2-day holding periods than those that had been stored in air or the 40% O2 atmospheres, suggesting that there are residual decay protection in 60–100% O2 treated fruits. In blueberries, 40% O2treatment even significantly promoted fruit decay during the subsequent 2 days holding period in air at 20 °C. High O2 atmospheres, alone or in combination with high CO2, have also been shown to inhibit fungal growth and decay
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Table 1 Effect of high O2 atmospheres on Chinese bayberry fruit decay after 9 days of storage at 5 °C and after an additional 1 and 2 days in air at 20 °Ca Treatment
Decay (%) 9 days at 5 °C
Decay (%) 9 days at 5 °C plus 1 day in air at 20 °C
Decay (%) 9 days at 5 °C plus 2 days in air at 20 °C
Air 40% O2 60% O2 80% O2 100% O2
21.1a 22.2a 12.2b 8.89c 7.78c
43.9a 41.7a 28.5b 25.6b 16.8c
83.9a 82.7a 54.7b 51.9b 36.2c
a Data are expressed as mean of triplicate assays. Values in the same column having the same letter are not significantly different at p 6 0.05.
incidence in other studies. In strawberries, Wszelaki and Mitcham (2000) reported that there was a decrease in fruit decay with an increase in oxygen concentration above 40%. The 90% O2 and 100% O2 treatments had significantly less fruit decay than either the 15% CO2 itself or in combination with 40% O2 after 14 days of storage at 5 °C. Pe´rez and Sanz (2000) found that 100% O2 or 80% O2 in combination with 20% CO2 were more effective in controlling fungal decay than the conventional CA during storage at 8 °C. Fruit decay was also significantly reduced by high O2 modified atmosphere packaging (70% O2) compared with conventional MAP in strawberry and raspberry during storage at 7 °C (Van der Steen, Jacxsens, Devlieghere, & Debevere, 2002). However, the mechanisms by which high O2 atmospheres inhibit fruit decay are yet unclear. It is possible that atmospheres containing higher than 40% oxygen are toxic to decay microorganisms, due to the unfavorable effects of high oxygen on the oxidation–reduction potential of the system, the oxidation of certain enzymes especially those having sulfhydryl groups or disulfide bridges and the accumulation of injurious reactive oxygen species (Fridovitch, 1975). Wszelaki and
Mitcham (2000) found that 80–100% O2 was more effective in suppressing strawberry fruit decay caused by Botritis cinerea infection than in inhibiting the in vitro growth of Botritis cinerea itself, suggesting that the high oxygen atmospheres have an effect on the fruit itself as well as the decay fungus, thereby resulting in greater effect in vivo than in vitro. Modification of storage atmospheres has been shown to induce plant defensive responses and increase disease resistance in postharvest commodities. Carbon dioxide conditioning of avocado fruit before storage promoted levels of antifungal compounds (eg epitachin) and consequently delayed decay development by Colletotrichum gloeosporioides (Prusky, Plumbley, & Kobiler, 1991). Similarly, natural resistance of mango fruit to Alternaria alternata increased in response to carbon dioxide treatment (Prusky, Kobiler, Zauberman, & Fuchs, 1993). Therefore, whether the induced plant defensive responses also involve in the inhibitory effect of high oxygen atmosphere on fruit decay observed in this and other studies remains to be investigated. 3.2. TA and TSS After 9, 14 or 35 days of storage at 5 °C, TA content in Chinese bayberry, strawberry and blueberry fruit, respectively, was significantly lower than the initial value. No significant differences in TA content were observed among all of the high O2 and air treated fruit in all the three berries (Tables 4–6). However, Pe´rez and Sanz (2000) found significantly lower TA content in strawberry fruit exposed to 90% O2 + 10% CO2 than fruit held in air after 9 days of storage at 8 °C. TSS decreased during storage in all three berries. No significant differences were observed in TSS content among all of the high O2 treated and control fruit in Chinese bayberry (Table 4), while high O2 levels P60%
Table 2 Effect of high O2 atmospheres on strawberry fruit decay after 14 days of storage at 5 °C and after an additional 1 and 2 days in air at 20 °Ca Treatment
Decay (%) 14 days at 5 °C
Decay (%) 14 days at 5 °C plus 1 day in air at 20 °C
Decay (%) 14 days at 5 °C plus 2 days in air at 20 °C
Air 40% O2 60% O2 80% O2 100% O2
27.7a 25.1a 13.5b 11.2b 8.25c
53.9a 51.7a 29.1b 24.3b 17.4c
76.4a 72.7a 51.2b 49.9b 37.3c
a
Data are expressed as mean of triplicate assays.Values in the same column having the same letter are not significantly different at p 6 0.05.
Table 3 Effect of high O2 atmospheres on blueberry fruit decay after 35 days of storage at 5 °C and after an additional 1 and 2 days in air at 20 °Ca Treatment
Decay (%) 35 days at 5 °C
Decay (%) 35 days at 5 °C plus 1 day in air at 20 °C
Decay (%) 35 days at 5 °C plus 2 days in air at 20 °C
Air 40% O2 60% O2 80% O2 100% O2
40.3a 39.2a 19.5b 6.66c 4.49c
54.8b 62.7a 42.1c 22.9d 17.5d
67.5b 73.1a 47.7c 31.2d 25.4e
a
Data are expressed as mean of triplicate assays. Values in the same column having the same letter are not significantly different at p 6 0.05.
Y. Zheng et al. / Food Control 19 (2008) 470–474 Table 4 Effect of high O2 atmospheres on Chinese bayberry fruit quality during storage at 5 °Ca Day and treatment
TA (%)
TSS (%)
L*
Hue angle
Day 0 Day 9 air 40% O2 60% O2 80% O2 100% O2
0.77 0.66a 0.67a 0.67a 0.67a 0.68a
10.1 8.7a 8.9a 8.8a 8.9a 8.9a
22.1 22.4a 22.5a 23.6a 23.7a 23.1a
18.3 17.5a 17.2a 18.5a 18.8a 18.4a
a
Data are expressed as mean of triplicate assays for TA, TSS and of 30 assays for L* and Hue angle. Values in the same column having the same letter for day 9 are not significantly different at p 6 0.05.
Table 5 Effect of high O2 atmospheres on strawberry fruit quality during storage at 5 °Ca Day and treatment
TA (%)
TSS (%)
L*
Hue angle
Day 0 Day 14 air 40% O2 60% O2 80% O2 100% O2
0.76 0.66a 0.65a 0.66a 0.65a 0.67a
7.8 6.0b 5.8b 5.9b 6.3a 6.4a
42.7 43.2a 43.4a 43.9a 43.1a 42.8a
49.8 49.1a 49.1a 49.2a 48.4a 48.4a
a Data are expressed as mean of triplicate assays for TA, TSS and of 30 assays for L* and Hue angle. Values in the same column having the same letter for day 14 are not significantly different at p 6 0.05.
Table 6 Effect of high O2 atmospheres on blueberry fruit quality during storage at 5 °Ca Day and treatment
TA (%)
TSS (%)
L*
Hue angle
Day 0 Day 35 air 40% O2 60% O2 80% O2 100% O2
0.82 0.44a 0.41a 0.43a 0.44a 0.45a
11.0 8.5b 8.3b 9.0a 9.2a 9.5a
32.4 30.4a 30.5a 30.8a 30.5a 30.7a
5.72 308b 312b 334a 340a 341a
a Data are expressed as mean of triplicate assays for TA, TSS and of 30 assays for L* and Hue angle. Values in the same column having the same letter for day 35 are not significantly different at p 6 0.05.
tended to maintain higher TSS values than did 40% O2 and air in strawberry and blueberry fruit (Tables 5 and 6). After 14 days of storage at 5 °C, significantly higher values of TSS in 80% or 100% O2 treated strawberry fruit were detected in comparison with other high O2 and air treatments. After 35 days of storage at 5 °C, significantly higher values of TSS in three higher level O2 treated blueberry fruit were detected in comparison with 40% O2 and air treatments. However, no significant differences were observed in TSS between the two or among the three higher level O2 treatments in strawberry or blueberry fruit. On the contrary, significantly lower TSS values in high O2-treated strawberries than in air-stored fruit after storage at 5 °C were reported in earlier studies (Wszelaki & Mitcham, 2000; Pe´rez & Sanz, 2000). As the main substrates of respiratory metabolism, sugars and acids are depleted
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causing corresponding changes in TSS and TA during storage. It has been shown that exposure of harvested horticultural crops to superatmospheric O2 levels may stimulate, have no effect on, or reduce rates of respiration, depending on the commodity, maturity stage, time and temperature of storage, and O2,CO2 and ethylene concentrations (Kader & Ben-Yehoshua, 2000). The different change patterns of TA and TSS in different fruits and studies seem to be associated with the different effects of elevated O2 on commodity respiratory rate. 3.3. Fruit color Chinese bayberry and strawberry fruit surface color did not change significantly during storage. After 9 or 14 days of storage at 5 °C, comparable L and hue angle values were found among all of the high O2 treated and the air control fruit in both berries (Tables 4 and 5). Similarly, no significant differences were observed in fruit color of strawberries stored under high O2 atmospheres compared to air stored fruit (Pe´rez & Sanz, 2000; Wszelaki & Mitcham, 2000). On the contrary, there was a significant decrease in blueberry fruit surface L-value after 35 days of storage at 5 °C, indicating that the fruit became darker with storage. Comparable L-values were found among different high O2 treatment groups and the air control group (Table 6). The hue angle, which gives a better indication of blueberry color, increased during storage. Significantly higher hue angle values, indicating more blue color, were detected in fruits stored at 60–100% O2 than in other treatments after 35 days of storage. Different change patterns of fruit surface color in Chinese bayberries, strawberries and blueberries were perhaps due to the differences in composition and concentration of phenolic compounds. 4. Conclusion In summary, the data presented in this paper indicate that high O2 atmospheres significantly affect Chinese bayberry, strawberry and blueberry fruit decay during and after cold storage, whereas fruit quality was only mildly affected by high O2. High O2 concentrations between 60% and 100% generally had significantly less decay during cold storage at 5 °C and subsequent 2 days holding period in air at 20 °C. Acknowledgements This study was supported by the National Natural Science Foundation of China (No. 30170661). We thank Dr. Chien Yi Wang of Produce Quality and Safety Laboratory, Beltsville Agricultural Research Center, USDA, USA, to critically reading the manuscript. References Allende, A., Jacxsens, L., Devlieghere, F., & Artes, F. (2003). Microbial and sensory quality of fresh processed lettuce salad under high O2
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