Reduction of postharvest rind disorders in citrus fruit by modified atmosphere packaging

Reduction of postharvest rind disorders in citrus fruit by modified atmosphere packaging

Postharvest Biology and Technology 33 (2004) 35–43 Reduction of postharvest rind disorders in citrus fruit by modified atmosphere packaging Ron Porat...

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Postharvest Biology and Technology 33 (2004) 35–43

Reduction of postharvest rind disorders in citrus fruit by modified atmosphere packaging Ron Porat∗ , Batia Weiss, Lea Cohen, Avinoam Daus, Nehemia Aharoni Department of Postharvest Science of Fresh Produce, ARO, Volcani Center, P.O. Box 6, Bet Dagan 50250, Israel Received 2 October 2003; accepted 8 January 2004

Abstract Citrus fruit are relatively non-perishable, and can normally be stored for long periods of 6–8 weeks. However, the development of various types of rind disorders limits the postharvest storage capability, and causes massive commercial losses. In the present study, we found that modified atmosphere packaging (MAP) in “bag-in-box” Xtend® films (XF) effectively reduced the development of chilling injury (CI) as well as other types of rind disorders that are not related to chilling, such as rind breakdown, stem-end rind breakdown (SERB) and shriveling and collapse of the button tissue (aging). In all cases, microperforated films (0.002% perforated area) that maintained CO2 and O2 concentrations of 2–3 and 17–18%, respectively, inside the package were much more effective in reducing the development of rind disorders than macroperforated films (0.06% perforated area), which maintained CO2 and O2 concentrations of 0.2–0.4 and 19–20%, respectively. In both types of package, the relative humidity (RH) was ∼95%. No major differences were found between the effectiveness of polyethylene (PE) and XF packages, despite the fact that XF prevents water condensation inside the bags. Overall, microperforated and macroperforated XF packages reduced rind disorders not related to chilling (rind breakdown, SERB and aging) after 5 weeks of storage at 6 ◦ C and 5 days of shelf life conditions by 75 and 50%, respectively, in ‘Shamouti’ orange, and by 60 and 40%, respectively, in ‘Minneola’ tangerines. Similarly, microperforated and macroperforated XF packages reduced the development of CI after 6 weeks of cold storage at 2 ◦ C and 5 days of shelf life conditions by 70 and 35%, respectively, in ‘Shamouti’ oranges and by 75 and 45%, respectively, in ‘Star Ruby’ grapefruit. Furthermore, storage of unwrapped ‘Shamouti’ oranges in high RH (95%) also reduced rind disorders by 40–50%, similarly to the effects of the macroperforated films. In the light of these data, we suggest that MAP reduces the development of rind disorders in citrus fruits via two modes of action: the first, which is common to both microperforated and macroperforated films is by maintaining the fruit in a high RH environment; the second, which is specific to the microperforated film, involves maintaining a modified atmosphere environment with elevated CO2 and lowered O2 levels. © 2004 Elsevier B.V. All rights reserved. Keywords: Chilling injury; Citrus; Modified atmosphere; Postharvest; Rind breakdown

1. Introduction



Corresponding author. Tel.: +972-3-968-3617; fax: +972-3-968-3622. E-mail address: [email protected] (R. Porat).

Citrus fruit are non-climacteric, with persistently low respiration and ethylene production rates, do not undergo any major softening or compositional changes after harvest and, therefore, can normally be stored for

0925-5214/$ – see front matter © 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.postharvbio.2004.01.010

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relatively long periods of 6–8 weeks (Kader, 2002). However, two major problems limit the long-term storage capability of citrus fruit: the first is pathological breakdown, leading to decay; the second is physiological breakdown, resulting in the appearance of various rind disorders. However, whereas it is practicable to solve the problem of decay development, either by the application of fungicides (Eckert and Ogawa, 1985) or by alternative environmental safe methods (Porat et al., 2002), there is not yet any reliable commercial method to alleviate the development of many kinds of rind disorder. Generally, the various rind disorders in citrus fruit can be divided into two main groups: chilling injuries (CI) that develop following storage at low sub-optimal temperatures; and other rind disorders, not related to chilling, that develop during storage at optimal non-chilling temperatures (Grierson, 1986; Kader and Arpaia, 2002). Chilling damage in citrus fruit may appear in various forms, such as browning of the flavedo (the outer pigmented layer of the peel) as in oranges (Fig. 1D), browning of the albedo (the inner white layer of the peel) as in lemons, appearance of dark sunken areas of collapsed tissue (pitting) as in grapefruit, and ‘watery breakdown’ as in oroblanco (Grierson, 1986; Porat, 2003). Other peel disorders, that are not related to chilling, include rind breakdown (Fig. 1A), stem-end rind breakdown (SERB) (Fig. 1B), and the shriveling and collapse of the stem-end button that indicates aging (Fig. 1C). Several postharvest horticultural treatments, such as intermittent warming, application of heat treatments, high- and low-temperature conditioning, etc., have been developed to reduce CI disorders in citrus fruit (Porat et al., 2000; Porat, 2003). Nevertheless, as far as we are aware, no commercial treatments are yet available to reduce the development of other rind disorders that occur under optimal, non-chilling temperature conditions. One possible means to reduce the development of rind disorders in citrus fruit may be the use of modified atmosphere packaging (MAP), by placing the fruit in “bag-in-box” plastic liners (Kader et al., 1989). Thus, it has been shown that by a single prestorage exposure to high CO2 levels (20–40% CO2 for 3 days), it is possible to reduce the development of some forms of rind disorders (Hatton and Cubbedge, 1977). Furthermore, it has been suggested that the development

of some types of rind disorders that are not related to CI, such as rind breakdown and SERB, may be enhanced by increased water loss from the peel tissue (Albrigo, 1972; Vercher et al., 1994). Therefore, MAP provides two advantages: it modifies the atmosphere inside the package to the O2 and CO2 levels required to alleviate the development of rind disorders, and it maintains a high humidity environment for the commodity inside the plastic film (Kader et al., 1989). The modified humidity atmosphere retains fruit freshness (Ben-Yehoshua et al., 1996; Tugwell and Chvyl, 1996) and, thus, may eliminate the development of rind disorders caused by water loss. Indeed, it was recently demonstrated by Ben-Yehoshua et al. (2001) that by providing high humidity conditions using MAP with polyethylene (PE) liners, it was possible to reduce the development of specific rind blemishes (superficial flavedo necrosis, locally known as ‘nuxan’) in ‘Shamouti’ oranges. Nevertheless, it should be noted that build up of severe anaerobic conditions in the internal atmosphere of the fruit, which may occur, for example, after waxing and storage at high temperatures or by inappropriate MAP, may promote the development of rind disorders (Petracek et al., 1998). Development of postharvest rind disorders causes severe economic losses to the entire citrus industry worldwide (Ceponis, 1986). In Israel, in particular, the fresh citrus industry suffers from the development of various rind disorders, such as CI, that occasionally develop in grapefruit and oroblanco, following the cold disinfestation treatments required to export the fruit to fly-free zones where quarantine regulations operate. Other disorders, not related to chilling, such as rind breakdown, SERB and aging, often develop on ‘Shamouti’ oranges and ‘Minneola’ tangerines, and also, occasionally after long-term storage, on ‘Valencia’ oranges. As part of an ongoing research project in our laboratory, aiming to reduce the development of postharvest rind disorders in citrus fruit, we examined the effects of MAP on the development of rind disorders following storage at either optimal or chilling temperatures. The data presented in this study clearly show that, in addition to its role in maintaining freshness, MAP significantly reduced the development of postharvest rind disorders and, therefore, might be used as a commercially practical means to maintain fruit quality.

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Fig. 1. Postharvest rind disorders of ‘Shamouti’ oranges: (A) rind breakdown; (B) SERB; (C) aging; (D) CI.

2. Materials and methods 2.1. Plant material and storage conditions ‘Shamouti’ oranges (Citrus sinensis Osbeck), ‘Minneola’ tangerines (Citrus reticulata Blanco) and ‘Star Ruby’ grapefruit (Citrus paradisi Macf.) were obtained from commercial packinghouses and used on the day after harvest. For all experiments, fruit were harvested during the period from late December until mid January. Standard packinghouse treatments included dips in hot imazalil (250 ␮l l−1 at 50 ◦ C) and coating with a commercial ‘Zivdar’ polyethylene-based wax (Safe-Pack Ltd., Israel). For the evaluation of rind disorders, ‘Shamouti’ oranges and ‘Minneola’ tangerines were stored at 6 ◦ C for 5 weeks and then transferred to shelf-life conditions at 20 ◦ C for 5 days. For the evaluation of CI, ‘Shamouti’ oranges and ‘Star Ruby’ grapefruit were stored at 2 ◦ C for 6 weeks and then transferred to shelf-life conditions at 20 ◦ C for 5 days. The relative humidity was 85% in all storage rooms.

The experiments were conducted during four consecutive seasons (from 1998 to 2002), and each experiment was repeated at least two or three times. Among the various experiments, each treatment comprised four replicate boxes, each containing 45 oranges (total of 180 fruit per treatment), 70 tangerines (total of 280 fruit per treatment) and 35 grapefruit (total of 140 fruit per treatment). 2.2. Packaging treatments Upon arrival at the laboratory, fruit were repacked in the same cartons within 90 cm × 90 cm plastic liners (“bag-in-box” package type), which were tightly closed with rubber bands. The control fruit were packed in cartons without plastic liners. The plastic liners used included 20 ␮m thick Xtend® films (XF10, XF12, XF14) and low-density polyethylene films (PE) (StePac LA, Tefen, Israel). According to the manufacturer’s specifications, the proprietary blends of polymeric materials composing the Xtend® films and PE films had O2 perme-

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ances of 24 × 10−14 and 35 × 10−12 mol s−1 m−2 at 23 ◦ C, respectively. The water vapor transmission rates (WVTRs) of the XF10, XF12, XF14 and PE films were 18 × 10−10 , 6 × 10−10 24 × 10−10 and 11.8 × 10−11 mol s−1 m−2 Pa−1 , respectively. The gas permeance of the XF and PE packages depended on the degree of perforation, which expresses the total area of the pores as a percentage of the film surface area, which was 0.002 and 0.06% for microperforated and macroperforated films, respectively. After transfer to shelf-life conditions at 20 ◦ C, the rubber bands were removed and the bags were opened.

was measured by titration with 0.1 N NaOH to pH 8.3, the results being expressed as citric acid percentages. Furthermore, at the end of each storage period, a taste score was evaluated by a panel of 10 trained tasters. 2.7. Statistical analysis Results were analyzed with the SigmaStat statistical software (Jandel Scientific Software, San Rafael, CA, USA). Student–Newman–Keuls one-way analysis of variance (ANOVA) tests on ranks were performed, and the results reported are significant at P < 0.05.

2.3. Atmosphere analysis 3. Results Samples of headspace atmospheres were withdrawn from the packages into gas-tight syringes through silicone septa attached to the film surface, and the concentrations of O2 and CO2 were determined with a Packard 7500 gas chromatograph (Packard, IL, USA) equipped with a thermal conductivity detector and a CTR-I packed column (6 ft length and outer diameter of 1/4 in.) (Alltech, USA), and with helium used as a carrier gas. 2.4. Measurements of RH and weight loss The RH in the packages was measured at the end of the cold storage period with a hygrometer (HD 8501H, Delta OHM, Italy), by inserting the probe into a small hole in the bag. Each measurement was done after 30 min of equilibration. In addition, 15 fruit per treatment were weighed before and after storage to assess the percentage weight loss. 2.5. Evaluation of rind disorders At the end of the storage and subsequent shelf-life periods, fruit were sorted according to their type of rind disorder, as follows: none, rind breakdown, SERB, aging, and CI (Fig. 1). The final results are expressed as percentages of the total number of fruit examined, that exhibited the various rind disorders. 2.6. Fruit quality evaluation The total soluble solids (TSS) content in the juice was determined with a refractometer, and the acidity

The quality of citrus fruit is often impaired by the development of various types of disorders; the most common ones are rind breakdown, SERB, aging and CI (Fig. 1A–D). Preliminary observations showed that packing ‘Shamouti’ oranges within various XF (XF10, XF12, XF14) and PE liners markedly reduced the development of rind disorders following storage at optimal non-chilling temperatures (Fig. 2). No major differences were found between the effectiveness of the various XF and PE film types, but there was a significant difference in effectiveness between the microperforated and macroperforated films. Overall, packing the fruit in various XF and PE microperforated and macroperforated films reduced the total amount of rind disorders to only 3.2 and 7.1%, respectively, as compared with 13.8% in control unwrapped fruit (Fig. 2). Since XF has a higher WVTR than PE and therefore offered the advantage of avoiding water condensation inside the packages, we chose to use the XF10 liner in further experiments. XF10 is also the cheapest Xtend® liner and, therefore, is mostly recommended by the manufacturers for commercial use in citrus. Detailed evaluation of the effects of microperforated and macroperforated XF10 liners with ‘Shamouti’ oranges showed that they effectively reduced the development of various rind disorders not related to chilling—rind breakdown, SERB and aging—following 5 weeks of storage at 6 ◦ C and 5 days at shelf-life conditions, by 95, 55 and 93%, and by 60, 32 and 80%, respectively, as compared

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Fig. 2. Effects of various Xtend® and PE packages on the development of postharvest rind disorders in ‘Shamouti’ oranges. Fruit were kept unwrapped (control) or were packed in microperforated or macroperforated XF10, XF12, XF14 or PE liners. The percentage of rind disorders was measured after 5 weeks of storage at 6 ◦ C and 5 additional days of shelf-life conditions at 20 ◦ C. Data are means of three separate experiments, each containing 180 fruit per treatment. Columns marked by different letters are significantly different at P < 0.05 according to a Student–Newinan–Keuls one-way ANOVA test on ranks.

with control unwrapped fruit (Fig. 3). Similar results were obtained with ‘Minneola’ tangerines, in which microperforated and macroperforated XF10 liners reduced rind breakdown and aging, following 5 weeks of storage at 6 ◦ C and subsequent shelf-life, by 52 and 65% or 33 and 46%, respectively (Fig. 4). SERB disorders were not detected following storage of ‘Minneola’ tangerines. Furthermore, the microperforated and macroperforated XF10 liners also significantly reduced the development of CI disorders following 6 weeks of cold storage at 2 ◦ C and 5 days at shelf-life conditions, by 71 and 35%, respectively, in ‘Shamouti’ oranges; and by 75 and 45%, respectively, in ‘Star Ruby’ grapefruit (Fig. 5).

Analysis of the RH and gas atmosphere inside the packages revealed that the RH levels were similar and high (∼95%) in both the microperforated and macroperforated types of XF10 liners (Table 1). However, the microperforated XF10 liner enabled a modified atmosphere to form inside the package, with elevated CO2 and decreased O2 levels (2.4% CO2 and 17.8% O2 ), whereas the gas atmosphere composition inside the macroperforated XF10 film hardly changed and remained more or less similar to that of the ambient air (Table 1). In order to study the possible effects of the elevated RH levels inside the packages on fruit weight loss and on the development of rind disorders, we further examined the direct effects of storing unwrapped fruit in

Table 1 Effects of microperforated and macroperforated XF10 liners on the RH and gas atmosphere within “bag-in-box” packages and on weight loss of ‘Shamouti’ oranges Treatment

Control (unwrapped) Microperforated XF10 Macroperforated XF10

RH (%)

85 ± 1 95 ± 1 95 ± 1

Gas atmosphere (%)

Weight loss

CO2

O2

0 2.4 ± 0.3 0.3 ± 0.1

21 17.8 ± 0.4 19.8 ± 0.4

6.0 ± 0.5 2.2 ± 0.3 2.3 ± 0.3

Measurements of RH and O2 and CO2 levels were taken after 5 weeks of storage at 6 ◦ C. Fruit weight loss was measured after 5 additional days of storage at shelf-life conditions at 20 ◦ C. Data are means ± S.E. of four replications, and are from one of several experiments with similar results.

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Fig. 3. Effects of microperforated or macroperforated XF10 packages on the development of various postharvest rind disorders in ‘Shamouti’ oranges. Fruit were kept unwrapped (control) or were packed in microperforated or macroperforated XF10 liners. The percentages of rind breakdown, SERB, aging, and total rind disorders were measured after 5 weeks of storage at 6 ◦ C and 5 additional days of shelf-life conditions at 20 ◦ C. Data are means of three separate experiments, each containing 180 fruit per treatment. Columns marked by different letters are significantly different at P < 0.05 according to a Student–Newman–Keuls one-way ANOVA test on ranks.

a high RH environment, and of waxing, which also reduces weight loss, on the development of postharvest rind disorders in ‘Shamouti’ oranges. It was found that waxing, which reduced weight loss from 6.0 to 4.1%, also reduced the development of rind disorders from 28.2 to 13.5% (data not shown). Furthermore, storage of waxed fruit in a high-RH environment (RH = 95%) reduced weight loss further, from 4.1 to 2.7%, and consequently reduced the development of rind disorders from 13.5 to only 6.6%. Thus, overall, storage of oranges in a high-RH environment and packing the fruit in macroperforated XF10 liners had similar effects on the development of rind disorders: the two

Fig. 4. Effects of microperforated or macroperforated XF10 liners on the development of various types of postharvest rind disorders in ‘Minneola’ tangerines. Fruit were kept unwrapped (control) or were packed in microperforated or macroperforated XF10 liners. The percentages of rind breakdown, aging, and total rind disorders were measured after 5 weeks of storage at 6 ◦ C and 5 additional days of shelf-life conditions at 20 ◦ C. Data are means of three separate experiments, each containing 280 fruits per treatment. Columns marked by different letters are significantly different at P < 0.05 according to a Student–Newman–Keuls one-way ANOVA test on ranks.

treatments reduced the development of rind disorders by 51 and 53%, respectively. On the other hand, microperforated XF10 packages, which also modified the gas atmosphere inside the package (Table 1), had a beneficial effect, and reduced the development of postharvest rind disorders by 75%, as compared with waxed unwrapped fruit (Fig. 2). Beside reducing the development of rind disorders and retaining freshness, the tested microperforated and macroperforated XF10 liners had no significant effects on other fruit quality parameters, including decay development, juice TSS and acid content, and fruit taste (data not shown).

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Fig. 5. Effects of microperforated or macroperforated XF10 liners on the development of CI in ‘Shamouti’ oranges and ‘Star Ruby’ grapefruit. Fruit were kept unwrapped (control) or were packed in microperforated or macroperforated XF10 liners. The percentages of CI were measured after 5 weeks of storage at 2 ◦ C and 5 additional days of shelf-life conditions at 20 ◦ C. Data are means of three separate experiments, each containmg 180 oranges or 140 grapefruit per treatment. Columns marked by different letters are significantly different at P < 0.05 according to a Student–Newman–Keuls one-way ANOVA test on ranks.

4. Discussion The susceptibility of citrus fruit to rind disorders may depend on various preharvest and postharvest factors. Factors that have been reported to affect the development of rind staining in oranges include: the rootstock variety (Zacarias et al., 2000) nutritional imbalances involving nitrogen and potassium fertilization (Wardowsky and Petracek, 1995; Tamim et al., 2001) endogenous content of growth regulators (Lafuente and Sala, 2002), and weather conditions during fruit development and at the time of harvest (Agusti et al., 2001). In addition, various studies found a correlation between the postharvest handling practices and storage conditions, on the one hand, and the development of rind breakdown, on the other. For example, in Florida, in order to reduce rind breakdown it was recommended to wax the fruit as soon as possible after harvest and to store them under high humidity (RH > 90%) (Hopkins and McCornack, 1960; Ritenour and Dou, 2002). Furthermore, it

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was reported that waxing, which reduces water loss, also reduced CI in grapefruit (Davis and Harding, 1959), and that seal packaging or wrapping the fruit in plastic bags reduced rind breakdown in oranges (Ben-Yehoshua et al., 2001). Packing fruit and vegetables in plastic bags offers several advantages, such as protecting the produce from mechanical damage and contamination, reducing moisture loss, and allowing modification of the gas atmosphere in the package (Hardenburg, 1971; Kader et al., 1989). However, MAP may also have detrimental effects. For example, the modified atmosphere inside the package may enhance anaerobic respiration and development of off-flavours, and the excessive humidity may increase decay incidence. Regarding citrus fruit, it has been reported that MAP may be used commercially to extend shelf life, to maintain freshness and to reduce weight loss (Ben-Yehoshua et al., 1996; Tugwell and Chvyl, 1996; D’Aquino et al., 1998). Nevertheless, citrus fruit are relatively sensitive to modified atmosphere conditions, and should not be stored under atmospheric environments containing less than 5% O2 or more than 5–10% CO2 (Davis et al., 1973; Kader et al., 1989; Ke and Kader, 1990). In the present study, we found that besides reducing weight loss in citrus fruit (Table 1), MAP also effectively reduced the development of various forms of rind disorders, including rind breakdown, SERB, aging and CI (Figs. 3–5). Similar findings regarding the effectiveness of MAP treatments in reducing CI in limes and grapefruit, as well as in other commodities, such as cucumber and mango, have been reported elsewhere (Wardowsky et al., 1973; Wang and Qi, 1997; Pesis et al., 2000). Nevertheless, in the present study, we found that MAP seemed to have a much broader effect in reducing the development of rind disorders, and that in addition to reducing CI (Fig. 5), it also effectively reduced the development of other forms of rind disorders that are not related to chilling, but occur also upon storage at optimal temperatures (Figs. 3–4). Thus, MAP presents some effects of generally strengthening the rind tissue and preventing its breakdown under various storage conditions. In contrast to MAP, other treatments that reduce CI, such as temperature conditioning and hot water rinsing and dipping (Porat et al., 2000), had no major ameliorative effects on other rind disorders (data not shown).

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In all experiments, we found that microperforated films, which maintained an atmospheric composition of 2–3% CO2 and 17–18% O2 inside the package, were much more effective in reducing the development of rind disorders than macroperforated films, which held an internal gas atmosphere with a composition more or less similar to that of the ambient air (Table 1, Figs. 2–5). However, it should be noted that packing citrus fruit in sealed or less perforated XF or PE liners with an atmosphere inside the package containing more than 7–8% CO2 or less than 14–15% O2 led to the development of off-flavours, and thus impaired fruit quality (data not shown). Therefore, when choosing a film type for citrus fruit, it is important to select the correct perforation area in order to achieve the desired modified atmosphere composition that will reduce rind breakdown but that will not impair fruit quality. Similar to our present findings, quite similar modified atmospheres containing 3 and 16%, and 5 and 10% of CO2 and O2 , respectively, were effective in reducing CI in cucumber and mango, respectively (Wang and Qi, 1997; Pesis et al., 2000). Overall, in the present study, we demonstrated that by using microperforated XF10 “bag-in-box” packages it is possible both to retain fruit quality and freshness and to reduce the development of various types of postharvest rind disorders. Nevertheless, special care should be taken in order to use only high quality fruit and to maintain the correct temperature during storage and transport in order to avoid the possible development of decay and of anaerobic respiration and off-flavours. The high water vapor permeability of the XF packages provides an important advantage for commodities that are sensitive to excess condensed water inside the package, as usually occurs in PE packages. Indeed, different versions of XF packages have been previously recommended for commercial storage of trimmed cucumbers, squash, Charentais-type melons, sweet corn, snap beans and mangoes (Rodov et al., 1998; Rodov et al., 2000; Rodov et al., 2002; Pesis et al., 2000; Fallik et al., 2002).

Acknowledgements We thank Dr. A. Sabehat and Mr. A. Shachnai from StePac LA., Ltd. for their assistance. This research was supported by grant number 401-0347-02 from

the Israel Citrus Marketing Board. The manuscript is a contribution from the Agricultural Research Organization, the Volcani Center, Bet Dagan, Israel, No. 414/03, 2003 series.

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