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Decay incidence and quality of different citrus varieties after postharvest heat treatment at laboratory and industrial scaleJuan F. García, Manuel Olmo and José M. García*Instituto de la Grasa (CSIC), Departamento de Fisiología y Tecnología de Productos Vegetales, Carretera Sevilla – Utrera Km 1, Campus de la Universidad Pablo de Olavide, Edificio 46, 41013 Seville, Spain* Corresponding author. Tel: +34954611550; Fax: +34954616790 Email: jmgarcia@cica.esAbstractMandarins (Fortune, Ortanique, Ellendale, Clemenules and Hernandina) and oranges (Navelate, Navelina, Lanelate, Salustiana and Valencia) were inoculated with the fungi Penicillium digitatum and Penicillium italicum and then subjected to postharvest heat treatment at laboratory scale by dipping in water at various temperatures for different treatment times before storage. 53?C (45?C for varieties showing mottled fruits after heat treatment at 53?C) and 3 min were found to be the most suitable conditions regarding decay incidence reduction, which were selected for the assays at industrial scale by using a heat water showers system in a commercial orchard. Heat treatment significantly reduced firmness and decay incidence in fruits after 5-day storage at 5?C and 7 days of shelf life at 20?C, and induced a delay in the evolution of skin colour. Other main quality parameters, such as juice content, soluble solids, pH, titratable acidity and sensory quality were unaffected. It was demonstrated that hot water postharvest treatments may be implemented in the citrus industry to extend shelf-life of fruits.Keywords: Hot water shower, Mandarins, Oranges, Penicillium digitatum, Penicillium italicum, Shelf-life1. IntroductionCitrus are one of the most widely produced fruits. They are grown for commercial purposes (mainly as fresh fruit and juice) in more than 137 countries around the world (Ismail and Zhang, 2004). Furthermore, citrus industry, including harvesting, handling, transport, marketing and delivery, is responsible for millions of jobs around the world and provides enormous benefits. Citrus fruits are beneficial for human consumption because of their nutritional and antioxidant properties. However, their higher water content and nutrient composition make them susceptible to infection by microbial pathogens, mainly fungi, from when they are harvested to their consumption (Talibi et al., 2014). This causes considerable losses to citrus producers. Penicillium digitatum (green mold) and Penicillium italicum (blue mold) are the major pathogens of citrus fruits. Both pathogens can infect citrus in the grove, the packinghouse and during distribution and marketing, the source of fungal inoculum being practically continuous during the season (Palou et al., 2008). Green mold can be reduced by storage at low temperatures. In general, mandarins are stored at 5-8°C while oranges at 4-8°C, with relative humidity of 90-95%, during cold storage (Kader, 2002). Decay incidence of citrus also increases with increasing storage period, which could be as high as 50% (Abd-El-Aziz & Mansour, 2006). Fruit decay is nowadays managed principally by the application of chemical fungicides, such as benzimidazole (thiabendazole, benomyl and carbendazim), sterol inhibitors (imazalil, prochloraz and propiconazole), sodium orthophenyl phenate and different mixtures of these compounds (Eckert and Brown, 1986; Eckert, 1990; Palou et al., 2008; Talibi et al., 2014), with the subsequent health hazards and environmental pollution. Besides, continuous use of fungicides may result in increasing fungicide resistance, which further complicates the management of fruit decay. What is more, the increasing spread of high-value markets based on sustainable, environmentally friendly, ecological or green agriculture makes even more necessary the use of alternatives to fungicides for citrus decay control (Palou et al., 2008).In order to prevent citrus decay and extend their shelf-life, some alternative postharvest treatments have been proposed, including physical treatments (curing, hot water and irradiation treatments), chemical treatments (sodium bicarbonate, calcium polysulfide and ammonium molybdate treatments, borax baths, and addition of natural compounds such as volatiles and essential oils, plant extracts, peptides, proteins, chitosan and chitosan derivatives), biological treatments (utilisation of microbial antagonists, application of naturally derived bioactive compounds and induction of natural resistance) and combinations of the above-mentioned treatments for integrated disease management (Palou et al., 2008; Talibi et al., 2014). Among them, heat treatments are regarded as the cheapest and most feasible technologies. Compared to other heat treatments such as curing, hot water treatments are easier, less expensive and more feasible for industrial scale (Palou et al., 2008). Relatively brief immersions (2–5 min) in hot water (45–55?C) have previously shown a potential in citrus green and blue moulds reduction (Schirra et al., 2004; Erkan et al., 2005; Palou et al., 2008).Changes in epicuticular wax ultrastructure have been observed on different citrus fruits subjected to postharvest heat treatments. Cuticular cracks disappeared as a consequence of the wax “melting” provoked by the hot water dip (Schirra et al. 2011). This facilitated the closure of this easy path for fruit infection and, consequently, reduced decay incidence. In addition, this improvement of the epithelial coating reduces fruit water loss by evaporation, which contributed to maintain quality traits and health-related properties (Palma et al. 2013; Kaewsuksaenga, et al. 2015).Despite the existence of numerous studies on alternatives to the use of fungicides in postharvest citrus, the control of postharvest losses due to infection by microorganisms in the citrus industry is still based on the application of fungicides. This may be due, first at all, to that such investigations have not achieved a sufficient decay control to compensate their application and replace synthetic fungicides. The aim of this research was to develop an industrial-scale hot water system for postharvest decay control without affecting the quality of fruits. To this end, 9 citrus varieties (5 mandarins and 4 oranges) were treated in a hot water showers system in a citrus industry, and decay incidence and quality parameters were monitored during storage and shelf life. Prior to this, the same varieties were treated in a hot water bath at laboratory to determine the most suitable treatment times and temperatures for each variety. The final objective was to effectively reduce citrus decay incidence at industrial facilities, without affecting fruit quality, and assess the shelf life of citrus.2. Materials and methods2.1. CitrusCitrus used throughout this research were grown in the commercial orchard "The Zumajo" located in Rio Tinto (Huelva, Spain) by the company Rio Tinto Fruit S.A. Citrus varieties used for the tests were mandarins (Fortune, Ortanique, Ellendale, Clemenules, and Hernandina) and oranges (Navelate, Lanelate, Salustiana and Valencia).2.2. Pathogen microorganismsThe fungi Penicillium digitatum and Penicillium italicum were obtained from the Spanish Type Culture Collection and maintained on potato dextrose agar plates. Conidia of a 7–12 days culture grown at 25°C were suspended in 100 mL sterile distilled water with two drops of Tween 80. The suspension was adjusted to 106 conidia/mL, using a haemacitometer. Fruits were wounded and inoculated on their flavedo using a 1.4 mm diameter steel rod, previously immersed in the conidia suspension. This concentration of pathogen was chosen because it has been verified that this amount is enough to provoke complete decay of citrus (Eckert and Brown, 1986) and it has been already successfully tested in a previous work (Nunes et al. 2007).2.3. Heat treatments at laboratory scaleAfter harvesting, citrus were let stand for one night at room temperature. Afterwards, 4 groups of 20 fruits each per citrus variety and pathogen were inoculated (i.e. 4 replicates per experiment). Two hours after the inoculation they were submerged for 30, 60, 90, 180 and 300 s at 40, 43, 45, 50, 48, and 53?C in thermostatically controlled water baths for heat treatments. At the same time, control was formed by another 4 groups with the same number of inoculated fruits per citrus variety and pathogen, which were not subjected to heat treatments. Finally, they were stored at 5?C for 5 days and then at 20?C for 7 days. During storage both losses by decay or physiological damage, and quality parameters of the fruits were monitored. These determinations were performed just after the heat treatment, after cold storage and after the period of shelf life.For non-destructive qualitative determinations (colour, firmness and weight loss) 20 fruits randomly taken from each treatment were selected at the beginning of the experiment, and the same fruits were measured in each sampling. For the destructive parameters (juice content, soluble solids, acidity and pH) 4 groups of 5 fruits per treatment and sampling were used, and the juice obtained from each group was considered as a replicate.2.4. Heat treatments at industrial scaleIndustrial-scale heat treatments were carried out at the facilities of the company Rio Tinto Fruit S.A. (Rio Tinto, Huelva, Spain). A batch shower system was used which was fed by a 5000-l thermostatic bath water by means of a pump with a flow capacity of 200 l/min. Pathogen inoculation was not performed in the industrial scale tests, and 2 water temperatures were assayed: 45 and 53?C. The procedure for each citrus variety was as follows: 16 packages of 20 kg fruit (not previously treated with fungicides) each one was simultaneously treated in the shower system with hot water for 180 s. Then they were stored for 5 days at 6 C and then an exhibition for sale at 20°C for a period of seven days was simulated. Losses due to decay and qualitative parameters of the fruits were monitored during both storage and shelf life periods. The determinations were performed at the beginning, at the exit of the cold room and after 7 days at 20°C. In each sampling 4 packages were extracted to assess the incidence of decay and the percentage of physiological damage, each package being a replicate. Complete decay of fruit was considered when there was visible growth of fungal mycelium. 5 fruits were randomly taken from each 20-kg package (i.e. 20 fruits per sampling since 4 replicates were performed) for destructive determinations. Another 5 random fruits per package were marked before heat treatment to monitor the non-destructive qualitative parameters during the whole process.2.5. Quality parametersDecay incidence was quantified by calculating the percentage of rotten citrus (fruits with visible mycelial growth) independently in each treatment.Colour index (CI), strongly related to degreening and ripening stage of citrus (Jiménez-Cuesta et al., 1981), was calculated from the CIELab parameters obtained by using a Minolta CR-200 handheld chroma meter (Konica Minolta Inc.) as follows:CI = 1000 · a* / L* · b*Fruit firmness (N/cm2) was measured by a Zwick 3300 hand densimeter (Zwick GMBH & Company, Ulm, Germany) and expressed in percentage of softening referred to fruit firmness before heat treatment. Similarly, weight losses were approximated as percent of original weight. Total soluble solids were determined according to AOAC (2005) using hand refractometer at room temperature, and expressed in ?Brix.As for juice content, 4 groups of 5 fruits per treatment were weighted. Then the fruits were cut in half and squeezed. The percentage of extracted juice was expressed as mL juice per 100 grams fruit.Finally, pH of fruits was measured with a digital pHmeter and total acidity was measured by titration method.2.6. Sensory analysis of the citrus juiceSensory analysis was solely performed in the assays at industrial scale by 10 panellists. The test consisted in ordering from best to worst quality two juice samples, the heat-treated one and the control. The sample of best quality was scored as "1" and the worst as "2". When a panellist did not find any difference in quality between samples, then it was given a score of "1.5". The scores by the panellists for each sample were summed to obtain a representative value of the quality thereof. Panellists were asked to pay particular attention to the possible occurrence of off-flavours. Each analysis was performed in duplicate.2.7. Statistical analysisAll the studied variables were analysed by ANOVA. When ANOVA detected a significant (p ≤ 0.05) effect due to each factor studied independently (temperature and storage time), a 5% level of least significant difference, calculated by Duncan’s multiple range test, was used to establish differences between the mean values. Both ANOVA and Duncan’s multiple range tests were calculated by using Costat 2.10 software (Cohort Software, Berkeley, USA). Sensory analyses were analysed by Friedman’s test to evaluate whether the ranking obtained had statistical significance (Land and Shepherd, 1988). The effectiveness of the treatment applied to decay incidence at industrial scale was performed using contingency tables and χ2 test with a 5 % of significance level.3. Results and discussion3.1. Decay incidence in laboratory scale assaysFirstly, heat treatment time was set to 180 s and different temperatures (40, 43, 45, 50 and 53?C) were assayed. Decay incidence after storage (5 days at 5?C and 7 days at 20?C) decreased as the treatment temperature was increased, being the treatments with water at 53°C the most effective against the development of pathogens (Tables 1 and 2). This temperature was similar to those pointed out by other authors for different fruits. Joseph and Aworh (1992) found that immersion of different varieties of mangoes in water at 55°C for 5 minutes resulted in a total reduction of decay losses after 8-day storage at temperatures between 26 and 29°C. Rodov et al. (1995) obtained a 50% reduction of decay losses in lemons and grapefruits treated by immersion in water at 53°C for 3 min. Similarly, Nafussi et al. (2001) inhibited the development of P. digitatum on lemon by immersing fruits in water at 52-53°C for 2 min. Nevertheless, none of these studies deals with the effect of heat treatments on fruit quality.In general, heat treatments at 53?C reduced decay development by 45–55%. However, in some citrus varieties, namely Navelate, Fortune, Elendale and Lanelate, the treatment at 53°C led to negative effect on the appearance of the fruit, leading to slight and moderate rind blemishes. This fact has been previously described by Palou et al. (2001) in Navelate oranges, which could be a hindrance for industrial application of water heat treatment at 53?C. For this reason, further heat treatments at both laboratory and industrial scale were performed at two different temperatures, namely 53 and 45?C. This latter temperature was selected to ensure a safety margin with respect to the quality of the fruit, despite losing effectiveness in preventing fruit decay.Secondly, another set of heat treatments was conducted to determine the most suitable treatment time. To this end, temperatures of 45 and 53°C were applied and citrus varieties Valencia and Clemenules were used. Decay reduction was greater as the duration of heat treatment increased (Table 3). Decay percentages under 50% were obtained after 3 min of heat treatment. Further decay reduction was achieved in heat treatments carried out for 5 min. Despite this, 3 min was considered as the most suitable treatment time, since there were not significant differences between the decay incidence obtained at 3 and 5 min. Furthermore, increasing for 2 min the treatment time would increase costs, being shorter heat treatments more feasible for industrial purposes. As for treatments shorter than 3 min, they reduced decay to some extent, but the percentages achieved were too high to be considered effective.3.2. Decay incidence in heat treatments at industrial scaleFruits thermally treated by the showers system at 53°C for 3 min showed lower decay incidence in citrus varieties used than untreated fruits (Table 4) although only in three of them there were significant differences (p ≤ 0.05). The low decay found in most fruits was a hindrance to obtain clear differences between treatments.A second set of industrial-scale assays was performed at 45°C with citrus varieties which were damaged in the laboratory-scale trials carried out at 53°C (Table 4). Very low incidence decay was obtained in both thermally treated and untreated citrus. Slight improvement was found when applying the showers system, but statistical analysis did not provide significant differences with control fruits.3.3. Effects on fruit quality3.3.1. ColourMost heat-treated fruits showed a slight delay in the colouring process. In Fortune, Ortanique, Clemenules, Navelate and Hernandina varieties the statistical study did show significant differences, both in laboratory scale trials (Tables 5 and S1-S8) and industrial scale assays (Tables 6 and S9-S16). The same differences found in Clemenules, Navelate and Hernandina varieties in the laboratory scale trials were found in the industrial scale assays. These results agree with those obtained by Kaewsuksaeng et al. (2015), who found that hot water treatment at 50 ?C for 5 min efficiently delayed the decrease of the contents of chlorophyll a and, consequently, of hue angle values of the lime fruit skin colour. This fact was related to the reduction of chlorophyll-degrading enzymatic activities induced by the postharvest hot water dips. Our results also agree with Smoot and Melvin's findings, who reported that the application of a water bath at 53°C for 5 min caused differences in the pigmentation of oranges (Smoot and Melvin, 1963), and differ from those published by Valero et al. (1998), who found that no significant delay occurred in the colour of lemons treated at 45°C for 10 min, and clearly opposed to Williams et al.’s results who obtained an increase of Valencia orange coloration after a treatment at 45°C for 42 min (Williams et al. 1994). 3.3.2. Fruit mottlingWhile untreated citrus showed no mottling regardless of the variety, the heat treatment at industrial scale at 53°C provoked a negative effect on the appearance of fruits of some varieties, leading to mottled fruits. To be specific, Navelate, Fortune and Elendale presented rind blemishes in about 40, 15 and 10%, respectively, of the fruit surface (Fig. 1) after 12-day storage (5 days at 5?C and 7 days at 20?C). The other varieties assays did not show this anomalous pigmentation. Pecina et al. (2007) observed, in a microscopic examination of the rind tissue of ‘Satsuma’ mandarins that had been previously dipped in hot water at 45 or 52 ?C, a change in the shape of the oil glands, without showing evidences of oil leakage or tissue damage after 8 weeks of cold storage (1?C) and 1 week of shelf life. In contrast, the non-treated fruit presented damaged tissue due to chilling with oil glands which did not have etheric oil. One year later, Ghasemnezhad et al. (2008), working also with ‘Satsuma’ mandarins, found that the major reduction of mottling incidence (chilling injury or heat damage) after 8 weeks of cold storage (2 ?C) was obtained in fruits previously dipped in hot water at 50 ?C for 2 min. However, temperatures higher than 50°C increased fruit peel damage. These authors related the severity of the mottling to the increase and the decline of peroxidase and catalase activities, respectively. Any enzymatic activity involved in the fruit physiology not only depends on the genetic information of each variety, but also on the particular cultivation conditions of each season and the post-harvest conditions, which include the ripening level at harvest, the storage and the conditions of shelf-life. This multiplicity of conditionings could explain the variability of results obtained by applying the same treatment to different citrus varieties or to fruits harvested at different seasons.3.3.3. Fruit softeningThe thermally treated fruits showed softening significantly lower than untreated citrus at the end of the exposure period for sale, both in laboratory scale trials (Tables 5 and S1-S8) and industrial scale assays (Tables 6 and S9-S16). These results are in agreement with those previously reported by Williams et al. (1994). Similarly to previous researches on avocado (Eaks, 1978), plum (Tsuji et al. 1984), tomato (Biggs et al. 1988), apple (Klein and Lurie, 1990) and strawberry (García et al., 1996), heat treatment led to subsequent hardening of the fruit. Heat treatments induce demethylation of pectin molecules from the cell wall and subsequent formation of salt bridges among such molecules thus enhancing consistency of cell wall (García et al., 1996). The composition of the citrus rind is therefore of major importance. When applying different edible coats to oranges, Shamloo et al. (2015) found that there were significant differences in fruit firmness after 3-month storage. Greater firmness in a fruit is a reliable indicator that such fruit will be more resistant to fungi infection. In this sense, heat treatment was not detrimental to citrus quality, quite the contrary.3.3.4. Weight LossesWeight losses increased over storage. Increased weight loss with increasing storage time is common in fruits, both in laboratory scale trials (Tables 5 and S1-S8) and industrial scale assays (Tables 6 and S9-S16). However, postharvest storage temperature also has a main influence on weight losses (Lee et al., 2015). Thus, Rab et al. (2012) assessed the effect of storage temperature (5, 10 and 20°C) on citrus fruits. The highest weight loss was found when fruits were stored at 20°C. Heat treatment by immersion in hot water causes a more homogeneous distribution of cuticular fruit waxes, covering the microfractures of the flavedo, thus interrupting this pathway of evapotranspiration. For this reason, this kind of treatment usually reduces weight losses or, at least, keeps them at the same level than the untreated fruit, unless the used temperature is not high enough to provoke this effect or, conversely, is excessive and causes heat damage (Schirra et al., 2011).3.3.5. Juice content, pH, soluble solids and titratable acidityWith regard to juice content, pH, soluble solids and titratable acidity, there were not significant differences between treated and control citrus, both in laboratory (Tables 5 and S1-S8) and industrial scale assays (Tables 6 and S9-S16). This is in agreement with other authors' findings. Porat et al. (2000) found no differences in soluble solids content in citrus after a short hot water brushing at 56, 59 and 62°C. Similarly, Shamloo et al. (2015) found that there were not significant differences in total acidity, total soluble solids, total sugar and pH between Valencia oranges treated with clove oil (1 %), wax or mixture of wax-clove oil and untreated oranges after 3-month storage at 7 °C and 85 % relative humidity. By contrast, Williams et al. (1994) obtained a reduction in acidity of Valencia oranges after heat treatment, and García et al. (1995) also reported a reduction in titratable acidity in strawberries treated at 35 and 45°C for 15 minutes. Other pretreatments, such as pasteurization, have been proved not to be able to modify orange juice content and its properties after storage either (Wibowo et al., 2015). Furthermore, it has been pointed out that postharvest storage temperature has not effect on mandarin juice content (Lee et al., 2015). In contrast to curing, which requires long time (3 days) of fruit exposure at a relatively high temperature, the treatment by immersion in hot water, which takes only few minutes, does not induce a significant increase of the respiratory rate in the fruit. This fact, together with the retention of weight losses, determines that fruit quality parameters such as juice content, titratable acidity and total soluble solids are barely modified by this postharvest treatment (Ghasemnezhad et al., 2008; Kaewsuksaeng et al., 2015).3.4. Sensory analysis of the citrus juiceSensory analysis did not show significant differences (Friedman test) among juice samples (data not shown). When asked, panellists did not find any negative effect of heat treatments at on fruit quality, developing neither atypical flavour nor off-flavour.ConclusionsThe extent of fungal growth in citrus inoculated with P. digitatum or P. italicum was inversely related to the temperature used in heat treatments at laboratory scale carried out at a fixed treatment time of 3 min. However, the application of the maximum temperature assayed (53?C) let to mottled fruits in Navelate, Fortune, Elendale and Lanelate varieties. The most suitable treatment time was found to be 3 min, which was selected for subsequent industrial scale assays. Increasing the treatment time up to 5 min did not significantly improve the reduction in the incidence decay. With regard to industrial scale assays, the application of hot water showers at 45?C to Navelate, Lanelate, Fortune and Elendale varieties, and at 53?C to Salustiana, Clemenules, Ortanique, Hernandina and Valencia varieties succeeded in reducing the natural decay incidence, although statistically significant differences were solely found for Clemenules, Hernandina and Valencia varieties. All citrus varieties subjected to heat treatment in water showers showed, at the end of the 7-day exposure period for sale at 20?C after previous storage of 5 days at 5°C, softening significantly lower than the untreated fruits. However, this treatment induced a delay in the evolution of skin colour. Instead, the juice content, soluble solids, pH, titratable acidity and sensory quality were unaffected. Based on the obtained results, an industrial application may be performed by inserting a set of water showers or a raft along the lines of postharvest handling, so that all the fruits are subjected to heat treatment in the most suitable conditions previously established for each variety.AcknowledgementsThe authors are grateful to the European Community (QLK5-1999-01065 and Interreg IIIA, Citrisaude, SP5. P120/03), and to INIA-Spain (CAL00-040-C2-01) for their financial support, to Rio Tinto Fruit SA (Huelva, Andalusia, Spain) for the technical assistance in commercial trials, and to M.C. Martínez for the technical assistance in the laboratory.ReferencesAbdel-El-Aziz S.A, Mansoor F.S. 2006. Some safe treatment for controlling post-harvest diseases of Valencia orange (Citrus sinensis L.) fruits. Annals Agric. Sci. 44: 135-146.AOAC. 2005. Official methods of analysis, 18th ed. 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