Changes in the oxidative state and nutrimental composition of orange residue (Citrus sinensis L.) dehydrated and ensiled at different timesABSTRACT
The aim was to evaluate the changes in oxidative state and chemical composition of orange residues dehydrated and ensiled at different times. Residues of fresh oranges after juice extraction were ground and divided into three parts, the first analyzed while fresh, the second dehydrated and the third ensiled in 7 plastic mini-silos and opened at 7, 14, 21, 28, 35, 42 and 49 days. Dry matter, crude protein, neutral detergent fiber, acid detergent fiber, pH, lactic acid, antioxidant capacity, phenols and flavonoids were measured. It was found that stabilization of lactic acid production occurred on day 28 of ensiling. The loss of dry matter and the increase of crude protein occurred from the 7th day to present later no changes; the process of fermentation during ensilage modified the antioxidant compounds, highlighting the increase (P<0.05) in the concentration of gallic, chlorogenic, vanillic, p-hydroxybenzoic and coumaric acids; the antioxidant capacity increased until reaching its maximum value on the 35th day of ensilage. Regarding dehydration, protocatechuic acid increased, while the other phenolic acids tended to disappear. It is concluded that the dehydration and ensilage of orange residues are dynamic processes that imply changes in the concentration of nutrients and antioxidants.
Keywords:
antioxidants; fermentation; phenols; flavonoids; ruminants
RESUMO
O objetivo deste estudo foi avaliar as alterações no estado oxidativo e na composição química de resíduos de laranja desidratados e ensilados em diferentes tempos. Os resíduos de laranjas in natura após extração do suco foram triturados e divididos em três partes, sendo a primeira analisada fresca, a segunda desidratada e a terceira ensilada em sete minissilos plásticos e abertos aos sete, 14, 21, 28, 35, 42 e 49 dias. Foram mensurados matéria seca, proteína bruta, fibra em detergente neutro, fibra em detergente ácido, pH, ácido láctico, capacidade antioxidante, fenóis e flavonoides. Verificou-se que a estabilização da produção de ácido láctico ocorreu no 28º dia de ensilagem. A perda de matéria seca e o aumento de proteína bruta ocorreram a partir do sétimo dia para posteriormente não apresentarem alterações; o processo de fermentação durante a ensilagem modificou os compostos antioxidantes, destacando-se o aumento (P<0,05) na concentração dos ácidos gálico, clorogênico, vanílico, p-hidroxibenzoico e cumárico; a capacidade antioxidante aumentou até atingir seu valor máximo no 35º dia de ensilagem. No que diz respeito à desidratação, o ácido protocatecuico aumentou, enquanto os demais ácidos fenólicos tenderam a desaparecer. Conclui-se que a desidratação e a ensilagem de resíduos de laranja são processos dinâmicos que implicam alterações na concentração de nutrientes e de antioxidantes.
Palavras-chave:
antioxidantes; fermentação; fenóis; flavonoides; ruminantes
INTRODUCTION
Due to the increase in the price of conventional ingredients used in animal feed, it is necessary to look for new alternatives that reduce their costs. The residues of oranges have been tested in the feeding of ruminants such as cattle (Allam et al., 2020), goats (Guzmán et al., 2020) and sheep (Volanis et al., 2004), and their inclusion in the diets has been found to be possible. In addition to the economic benefits that can be obtained by including orange residues to the diets of animals, this ingredient contains phenolic compounds (Montenegro-Landívar et al., 2021), which have antioxidant properties. In Mexico, orange production is concentrated in certain months of the year. Part of this production is destined for industry and the other part is for fresh consumption (Martínez-Jiménez et al., 2020). The extraction of the juice and part of the pulp produces residues with a high moisture content, which causes them to decompose in a short time. This makes it difficult to store them and use them continuously in animal feed, which is why it is necessary to preserve therefore, for these residues so that they can be used in animal feed. Ensilage and dehydration are widely used preservation methods for various fodders and byproducts for animal feed, the choice of which depends on the availability of resources and the most appropriate form for feeding to animals. When a product is conserved, the goal it is to improve or at least maintain its quality. These preservation methods can modify the antioxidant capacity of the product. During the ensiling process, there is an anaerobic fermentation stimulated by bacteria (Xu et al., 2018), which contributes to an increase in the concentration of phenolic compounds and flavonoids thanks to the microbial hydrolysis reaction due to the structural rupture of the cell walls (Hur et al., 2014). During dehydration, the high temperatures can alter the concentration of antioxidants, so their study is necessary to quantify these changes. There is sufficient evidence on the changes in nutritional quality such as protein, dry matter, minerals and energy during silage and dehydration (Łozicki et al., 2015; Kung et al., 2018); however, there is little information on the changes in antioxidants that may occur during the preservation process. Knowing these changes would help to determine whether the preservation of orange wastes potentiates, preserves or reduces their antioxidant properties and their use as an alternative antioxidant to counteract lipid oxidation. Therefore, the aim of the present study was to evaluate the changes in oxidative state and chemical composition of orange residues dehydrated and ensiled at different times.
MATERIALS AND METHODS
The residue of Valencia variety oranges (Citrus sinensis L.) was collected from two juice stands in the city of Oaxaca, Mexico. The residue consisted of seeds, peels and other parts except for juice, which had been extracted. After collection, the residue was crushed using a sieve with a diameter of 18 mm and, after homogenisation, 9 samples of approximately 4kg were taken.
The first sample was stored in a deep freeze at -80 °C until the corresponding analyses were carried out. The second sample was dehydrated at an average temperature of 45 °C for 4 days in a dehydrator covered with 720 caliber plastic, and the third to ninth samples were ensilaged in 7 plastic mini silos of 4 liters, to be uncovered later at 7, 14, 21, 28, 35, 42 and 49 days. The process of collection, fresh conservation, sun drying and ensiling at different times was repeated 7 times.
When the mini silos were opened, three samples were taken: the first of 50g was liquified to measure pH and lactic acid, the second was placed in a tray to be dehydrated in an oven at a constant temperature of 45°C for 48 h. When the time was up, the sample was placed in paper bags for subsequent bromatological analysis. The third sample of 100 g was placed in a plastic bag and deposited in a deep freezer at -80°C for the quantification of antioxidant capacity, flavonoids and phenolic acids.
To measure the pH of the fresh and ensiled orange residue, 50 g of sample was weighed and 100mL of distilled water was added. The residue was then crushed and filtered to obtain the extract, from which the pH was measured with a potentiometer (Thermo Scientific, model Orion 3 Star). From the extract used to measure pH, 4mL were taken to which 1mL of 25 % metaphosphoric acid was added. This mixture was used for the measurement of lactic acid according to the Taylor technique (1996).
Crude protein (CP) was determined by the method of Kjendhal (Association…, 2017), using the Foss KjeltecTM 8200 equipment. Acid detergent fiber (ADF) and neutral detergent fiber (NDF) were determined by the Van Soest method (1994).
An extract was obtained from each sample according to the method described by Rojas-Barquera and Narváez-Cuenca (2009). For this purpose, 0.5g of ground dry sample or 2g of ground wet sample were used, which were mixed with 10mL of methanol and water (50/50), acidified with HCl 2N to pH 2 and stirred with an orbital stirrer for 1 hour, then centrifuged at 3000 rpm for 15 minutes. The precipitate was treated with a mixture of 70% acetone and 30% water, vortexed and centrifuged in the same way as the first dilution. This second supernatant was collected and mixed with the first. The antioxidant capacity was determined using the ferric reduction antioxidant power (FRAP) method of Benzie and Strain (1996). The results were calculated using Trolox pattern curves dissolved in ethanol at different concentrations (0.2-1.6nM). The results were expressed as nmol Trolox per g dry matter.
The fresh and ensiled samples, kept in the deep freezer, were lyophilized in a freeze-dryer until the samples were dehydrated. Afterwards 0.150g of each sample were weighed, 3mL of 80% ethanol was added and the sample was placed in a double boiler with stirrer for two periods of 5 minutes and one rest period; then it was centrifuged for 5 minutes at 3000 rpm. One milliliter of the extract was placed in vials in a liquid chromatograph (Agilent model 1100), equipped with a model 1200 automatic injector and a diode array detector. The column was a Hypersil ODS 5µm particle diameter 125 x 4.0 mm from Agilent Technologies, the mobile phase was: A: water with 0.1% trifluoracetic acid and B: acetonitrile with 0.1% trifluoracetic acid. The analysis was performed by T gradient (0.10 min) 85% A, 15% B; T (20 min) 65% A, 35% B. The flow rate was 1.0 mL/min-1 at a temperature of 30 °C and the detector was set at 254 nm. To obtain the calibration curve of the flavonoids, 9 standards were used as reference such as hesperidin, rutin, phloridzin, quercetin, myricetin, naringenin, phloretin, apigenin and galangin.
For the determination of phenolic acids, a column was used: Nucleosil 100 A 125x 4.0mm d. i. 5 µm, Macherey-Nagel, flow, 1mL min-1; temperature 30°C; variable injection volume; and analysis time 25 min. Nine standards were used: protocatechuic acid, gallic acid, chlorogenic acid, syringic acid, vanillic acid, p-hydroxybenzoic acid, caffeic acid, ferulic acid and p-coumaric acid of Sigma-Aldrich, USA.
Tests for homogeneity of variance were performed using the Bartlett test and for normality with the Shapiro-Wilk test. When the data did not conform to homogeneity and normality of variance, transformations such as “Log” and “sqrt” were applied; later analyses of variance were performed with treatment as a fixed effect. Means were compared using the least significant difference test. The experimental unit was a plastic mini silo.
RESULTS
The silage showed a loss of dry matter (DM) during the first seven days (P<0.05), after which it remained stable. From day 14 of ensiling an increase in acid detergent fiber (ADF) was observed with respect to the fresh residue (P<0.05), while dehydration did not affect this variable (P>0.05). The mean values of neutral detergent fiber are more stable, but it was found that on the 28th day of ensilage, the percentage is higher than in the dehydrated residue. Dehydration and ensilage incremented the concentration of crude protein (P<0.05), with no difference (P>0.05) between the days of ensilage (Table 1).
At the time of ensiling, the pH was 2.40, it increased numerically (P>0.05) to 3.05 on day 7 and to 3.54 on day 14 of ensiling (P<0.05), from day 14 to 49 there was no difference (P>0.05). When comparing the concentration of lactic acid, it was observed that it increased during ensilage (P<0.05) until it was maintained on day 28 (Table 2), which could indicate that there was a stabilization on the anaerobic phase of fermentation after this day.
During the ensiling process, the antioxidant capacity increases with the days of ensiling until reaches its maximum value on day 35 (P<0.05), after which there is a tendency to decrease (Table 3). Similarly, there was tendency for dehydration to improve the antioxidant status. When comparing silage and dehydration, it was observed that dehydrated silage had a lower antioxidant capacity than on day 35 of fermentation (P<0.05), with no difference (P>0.05) with the other days of silage.
Eight of nine standards used were found: protocatechuic acid, gallic acid, chlorogenic acid, syringic acid, vanillic acid, and p-hydroxybenzoic acid, caffeic acid and p-coumaric acid (Table 4).
The phenolic acids showed changes during the ensiling process. A higher concentration of protocatechuic acid was observed in the dehydrated treatment (P<0.05) compared to the fresh and ensiled treatments (P>0.05). In contrast, gallic acid, vanillic acid, P-coumaric and p-hydroxybenzoic acids were not detected in the dehydrated sample. The p-hydroxybenzoic increase (P<0.05) during the ensilage process to reaches its maximum peak at day 28 and then decreased. Gallic acid, chlorogenic acid, vanillic acid and P-coumaric acid have their maximum peak between days 7 and 42 (P<0.05). Some, such as gallic acid and vanillic acid, tend to not be detected on day 49 of ensilage due to their low concentration in the fresh residue.
Six of nine standards used were found: hesperidin, rutin, phloridzin, quercetin, naringenin and galangin. Hesperidin was by far the most abundant antioxidant compound found in the orange residue, peaking on day 28. The percentages of phloridzin and naringenin did not change during dehydration and ensilage (P>0.05).
The concentrations of rutin, quercetin and galangin are similar (P>0.05) between the fresh and dehydrated treatments; in the ensiled treatment no trend was observed during the days of ensilage (Table 5).
DISCUSSION
Losses of DM during the fermentation process of ensilage are a problem and have been documented (Driehuis et al., 2001). The ensilage of the orange residue presented loss of dry matter from day 7, to remain stable later, this loss represented 13.57% of the ensiled orange residue. In previous works it was reported that the dry matter content of ensiled unmarketable ripe oranges mixed with other byproducts and hay decreased from 25 to 21% (Volanis et al., 2004). During the ensilage process, losses due to respiration, fermentation or effluents can occur, even reaching up to 13% of dry matter loss in poorly managed silage (Borreani et al., 2018). It is possible that dry matter loss recorded in the silage is due to the high moisture content of the orange peel. In this respect, it has been found that losses due to effluents and gases are reduced by including a fodder with a high dry matter content (Teixeira et al., 2013). These effluents contain organic compounds such as sugars, organic acids and proteins. In orange residue with 14.46% DM, the production of effluents decreases linearly with the inclusion of pelleted citrus pulp, while 20% of this pellet is required to reduce the production of gases (Kitagawa et al., 2020). Similarly, in elephant grass silage with 8.1% dry matter, it is possible to reduce gas and effluent losses by adding dry fodder to achieve a percentage of 24.2% to 28.3% of dry matter (Moura et al., 2010). The reduction of dry matter was rapid and appeared after 7 days, which indicates that these losses are rapid at the beginning of ensilage, given that later there were no losses, similarly Savoie et al. (2002) determined that the losses by effluents occurred within the first 7 days of ensilage, the decrease of dry matter can occur from the first day when the compaction of the silage is made.
Silage increased the percentage of crude protein from day 7, while ADF increased from day 14. In contrast, Du et al. (2020) found that the protein in silage decreased due to its degradation by some microorganisms and the subsequent increase in ammoniacal nitrogen content, thus reducing the quality of the silage. Savoie et al. (2002) determined that most of the effluents are composed of soluble sugars. Therefore, it is hypothesized that the increase in CP and ADF could be due to the loss of soluble components, leading to an increase in the concentration of these compounds in relation to the percentage of dry matter of the sample.
pH and lactic acid are two important indicators for measuring whether the fermentation of a silage has been adequate, as lowering the pH and increasing lactic acid inhibit the growth of undesirable bacteria. At the beginning of the ensiling process, it is common for the pH to be above the desired values, so the production of lactic acid by lactic acid bacteria (Kim et al., 2021) prevents the growth of undesired bacteria. At the beginning of ensilage, the orange residue has a high degree of acidity, which decreased rapidly and stabilized at 14 days, while the production of lactic acid stabilized at 28 days, which could indicate a stabilization of the anaerobic phase of fermentation from day 28. In this regard, Kung et al. (2018) mention that the final pH of maize silage is between 3.7 to 4.0 and that of legumes is between 4.3 to 5.0. While Kung (2018) mentions that the pH at the end of the fermentation process varies from 3.7 to 4.5, depending on the product to be ensiled and its dry matter; in addition, it must have a rapid pH drop that prevents the decomposition of proteins. Therefore, the present article demonstrates that the silage of orange residues has adequate values of pH and lactic acid content and within the normal parameters. For lactic acid to be produced, the product to be ensiled must contain the necessary amounts of water-soluble carbohydrates. Driehuis et al. (2021) evaluating Lactobacillus inoculation in Perennial ryegrass silage, found that dry matter losses and pH decrease occur mainly during the first 20 days of ensilage. According to the stabilization of the pH and lactic acid values, we can say that the ensilage of orange residues requires a minimum of 28 days.
With dehydration, there was a tendency to increase the antioxidant capacity, probably due to a very short fermentation process that takes place before dehydration. It has been shown that the dehydration of Citrus aurantium increases its antioxidant capacity (Covarrubias-Cardenas et al., 2018), just as the heating of Citrus unshiu extracts increments its antioxidant capacity (Jeong, 2004).
The antioxidant capacity increased with the number of days in the silo, reaching a maximum peak on day 35; similarly, the fermentation process increased the content of certain antioxidant compounds. In this regard, other authors have found that fermentation of a substrate improves the antioxidant status of the final product, for example, Sadh et al. (2018) found that during the fermentation with Aspergillus awamori, the content of total phenols and flavonoids increases, until reaching a peak at 120 h. However, there is a decrease at 144 h, during this period of fermentation, the bound phenol is released, causing an increase in the antioxidant capacity. Lee et al. (2008) found that fermentation of black beans increased the concentration of phenolic compounds and therefore their antioxidant capacity. Landete et al. (2014) showed that incubation with Lactobacilus plantarum increases antioxidant capacity, due to deglycosylation of the substrate. While Dordevic et al. (2010) mention that fermentation increases the levels of many bioactive compounds. During fermentation, lactic acid is produced, in this respect it has been found that these bacteria themselves have the capacity to synthesize antioxidants (Coda et al., 2012), in addition to promoting the release of phenolic compounds (López et al., 2013). Thus, the increase in antioxidant capacity of the orange silage during fermentation may be due to the increment in antioxidant compounds originally present in the sample or to the presence of compounds formed during the ensilage process. With respect to animal feed, there is scarce information on the modifications in the oxidative state during ensiling, so this study demonstrates that ensiling improves the antioxidant capacity of orange waste; therefore, it is a viable alternative to counteract lipid oxidation when incorporated in animal feed.
The principal secondary component found in the orange residue was hesperidin, which remained without a clear tendency to decrease or increase during the ensilage process. On the other hand, the gallic, chlorogenic, vanillic, p-hydroxybenzoic and p-coumaric acids increased with ensilage. Hesperidin has been shown individually to have antioxidant capacity (Al-Ashaal and El-Shelyawy, 2011). Although several phenolic acids such as gallic acid, P-hydroxybenzoic acid, P-coumaric acid disappeared during dehydration, it is possible that their high value of protocatechuic acid influenced the silage to show higher antioxidant capacity only on day 35, being similar with the other silage days.
In previous works it has been demonstrated that orange has a high value of antioxidant capacity and its content of hesperidin (Montenegro-Landívar et al., 2021). Covarrubias-Cardenas (2018) found that the type of solvent influences in the extraction and determination of the concentration of phenols, he also reports that in the peel of Citrus aurantium the naringin and neohesperidin are the most abundant phenols; in white Citrus reticulata the main compounds found are hesperidin, naringin, tangeritin and rutin, which represent 86% of the extracted phenolic compounds (Ferreira et al., 2018). In the residual water of orange residue, the main compounds found are narinutin (38.91 mg/l) and hesperidin (33.09mg/l) (Viuda-Martos et al., 2011).
Xiao-Yu et al. (2017) when fermenting buckwheat leaves with Aspergillus niger yeasts, demonstrated that the antioxidant capacity, total phenolic compounds, and rutin and quercetin increased linearly during the first 7 days; however, there was a strong reduction after day 7, which was attributed to enzymatic degradation of the antioxidant compounds. In orange silage, the antioxidant capacity increased to a maximum on day 35 and then decrease. Similarly, there are compounds such as hesperidin and p-hydroxybenzoic acid that increase with fermentation and later decrease on day 49 of ensilage; others such as gallic acid, vanillic acid and p-coumaric acid increase with fermentation and later are not detected on day 49, thus, although there is a stabilization in the silage with respect to its lactic acid content and pH, these secondary metabolites continue to present modifications during the storage period.
In previous studies we have found that there are physiological stages in animals where the antioxidant capacity in blood plasma decreases (Salinas-Rios et al., 2015; Salinas et al., 2017). The present study shows that orange waste contains a wide variety of antioxidant compounds, some of which are increased during ensiling process, thereby increasing its antioxidant capacity, making it not only a feed alternative due to its nutritional properties, but also an option to counteract lipid oxidation, especially when ensiled.
CONCLUSIONS
During the ensilage and dehydration of orange residues, changes occur in the content of nutrients and antioxidants, with a loss of dry matter from the first seven days of ensilage, while lactic acid stabilization occurs on day 28. Both preservation methods increase the percentage of crude protein. Regarding the presence of antioxidant, the most abundant antioxidant compound found in the orange residue was hesperidin, noting that silage increases the concentration of some antioxidant compounds such as gallic acid, chlorogenic acid, vanillic acid, p-hydroxybenzoic acid and p-coumaric acid, while dehydration increases the protocatechuic acid. Thus, ensiling of orange waste improves antioxidant capacity and dehydrating preserves it, both methods of conservation being an alternative for storing orange residue to be used in animal feed.
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Publication Dates
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Publication in this collection
21 Feb 2025 -
Date of issue
Mar-Apr 2025
History
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Received
13 Feb 2024 -
Accepted
23 July 2024
