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Inhibition of Melanosis in Whiteleg Shrimp (Litopenaeus vannamei) during Refrigerated Storage Using Extracts of Different Avocado (Persea americana Mill.) By-Products
1Faculty of Chemical and Food Technology, HCMC University of Technology and Education, Ho Chi Minh 70000, Viet Nam
2Research Center for Aquafeed Nutrition and Fishery Post-Harvest Technology (APOTEC), Ho Chi Minh 70000, Viet Nam
3Research Center of Ginseng and Medicinal Materials, National Institute of Medicinal Materials, Ho Chi Minh 70000, Viet Nam
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Prev Nutr Food Sci 2021; 26(2): 209-218
Published June 30, 2021 https://doi.org/10.3746/pnf.2021.26.2.209
Copyright © The Korean Society of Food Science and Nutrition.
Abstract
Keywords
INTRODUCTION
Whiteleg shrimp (
Melanosis in shrimp and other crustaceans is developed by the oxidation of phenol substrates (such as tyrosine in shrimp) to quinones catalyzed by polyphenolase, which generates dark pigments of high molecular compounds (Sae-leaw and Benjakul, 2019). From a commercial perspective, some methods have been used to prevent melanosis development in shrimp during storage, such as treatments with sulfite and phosphate compounds (Martínez-Álvarez et al., 2008; Galvão et al., 2017). However, the potential risks of using those chemical additives, i.e., nausea, abdominal pain, vomiting, and choking have raised awareness among customers and regulators. Consequently, researchers and scientists worldwide have recently paid considerable attention to natural, safe, and effective additives (Djeridane et al., 2006; Encarnacion et al., 2012). Natural antioxidant substances have been widely studied as substitutes to chemical additives to prevent melanosis. Natural additives, such as tocopherols, flavonoids, cinnamic acids, and coumarins were reported to exhibit potent antioxidant, antimicrobial, and polyphenoloxidase (PPO) inhibitory activities and thus, they could prevent the melanosis process (Gonçalves and de Oliveira, 2016). Plant extracts containing polyphenolic compounds demonstrated a significant retardation of melanosis formation in crustaceans, which was associated with tyrosinase inhibitory activity (Sae-leaw and Benjakul, 2019). Nirmal and Benjakul (2012) reported that the ethanolic extract of green tea containing a high amount of catechin and derivatives could significantly decrease the lipid oxidation and melanosis formation in whiteleg shrimp during cold storage. Encarnacion et al. (2012) prepared an extract of edible mushroom (
Recently, studies on utilizing agricultural by-products for food additives and preservation have been extensively investigated due to economic and environmental benefits (Gómez et al., 2014; Saavedra et al., 2017). Among various by-products, avocado seed and peel contained great amounts of phenolic compounds, including flavanol monomers, proanthocyanidins, hydroxycinnamic acids, and flavonol glycosides (Kosińska et al., 2012). This would attribute to a high potential of antioxidant activities of those by-products. Rodríguez-Carpena et al. (2011) showed that raw porcine patties treated with the extracts of avocado peel and seed could effectively inhibit lipid oxidation and color deterioration during chilled storage. Several studies also reported the applications of avocado by-products as potential sources of natural antioxidants or preservatives (Gómez et al., 2014: Saavedra et al., 2017; Gashahun and Solomon, 2018).
It is worth mentioning that avocado peel and seed are discarded as wastes, accounting for about 20% (w/w) of the fruit (Wang et al., 2010). Avocados are widely grown in Viet Nam, which has been considered as one of the seven important fruits crops in the country. Consequently, a large quantity of avocado by-products is discarded from fruit processing annually. Although the phenolic compounds, such as catechin, quercetin, and their derivatives from avocado by-products could exhibit a potential in preventing melanosis on crustaceans or shrimps (Nirmal and Benjakul, 2012; Qian et al., 2018; Tremocoldi et al., 2018; Rosero et al., 2019), to the best of our knowledge, there has been no report on utilizing avocado by-products as potential natural additives to prevent melanosis and/or extend the shelf life of whiteleg shrimp.
In this study, the roles of some popular avocado by-products on the retardation of melanosis and lipid oxidation in whiteleg shrimp during cold storage were evaluated and discussed. The study aimed to obtain three main objectives: (i) preparation of nine ethanolic extracts from by-products (seeds and peels) of three avocado varieties from Viet Nam, and determination of their total phenolic content (TPC) and antioxidant activities; (ii) evaluation of the capability of these prepared extracts in preventing melanosis formation and lipid oxidation in whiteleg shrimp during 8 days storage at 4°C; and (iii) discussion on the relationship between the inhibition on melanosis of these prepared extracts and their TPC values and antioxidant activities. The utilization of these by-products as food additives could not only reduce the negative impact on the environment but also expand the range of avocado value-added products.
MATERIALS AND METHODS
Materials and chemicals
Folin-Ciocalteu reagent, iron (III) chloride hexahydrate (FeCl3・6H2O), malondialdehyde (MDA), sodium metabisulfite (SMS), potassium hexacyanoferrate [K3Fe(CN)6], thiobarbituric acid (TBA), trichloracetic acid (TCA), gallic acid, kojic acid, 2,2-diphenyl-1-picrylhydrazyl (DPPH), and tyrosinase were purchased from Sigma-Aldrich Co. (St. Louis, MO, USA). All other chemicals were of analytical grade.
By-products (peels and seeds) from three popular varieties of avocado, namely ‘Nuoc’, ‘Sap’, and ‘034’ were supplied from several local markets in Ho Chi Minh City, Viet Nam. The samples were then dried to the moisture content of about 10% [using a gravimetric method followed by the European Brewery Convention (2000)]. The dried samples were subsequently ground in a blender into a homogenous fine pulp that was then extracted with ethanol.
Alive whiteleg shrimp with the size of 30∼40 shrimps/kg were purchased from Tan Binh market (Ho Chi Minh City, Viet Nam). The shrimps were immediately transported to the laboratory for the experiments.
Preparation of extracts
An extract of each avocado by-product was prepared using a maceration technique (Azwanida, 2015). Dried powder (30 g) was soaked in 100 mL of 70% ethanol (v/v) at 32°C for 24 h. The mixture was filtered to collect the extract solution, and the remaining residue was re-extracted with ethanol twice using the same procedure. Then, the mixture of three collected extracts was concentrated using a rotary evaporator to produce a crude extract. Table 1 presents the extraction yield (E%) of the nine prepared avocado by-product extracts. It includes three seed extracts and three peel extracts prepared from each variety [‘Sap’, ‘034’, and ‘Nuoc’: No. (1) to (6)], and three mixed extracts [No. (7) to (9)] consisting of peel mixture, seed mixture, and peel-seed mixture from 3 varieties mixed in equal weights. Note, the extraction yield (E%) can be calculated as in Eq. (1):
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Table 1 . The extraction yield of nine extracts prepared from by-products of three avocado varieties: ‘Sap’, ‘034’, ‘Nuoc’
No. Sample name Formulation/mixture Extraction yield (%) 1 SS Sap seed 12.5 2 SP Sap peel 10.0 3 OS 034 seed 10.1 4 OP 034 peel 7.6 5 NS Nuoc seed 18.1 6 NP Nuoc peel 7.8 7 MS Sap seed+034 seed+Nuoc seed 13.5 8 MP Sap peel+034 peel+Nuoc peel 7.6 9 MSP Mixture of all seeds and peels 9.8
where mextract is the weight (g) of the dried extract residue obtained after solvent removal, and mpowder is the weight (g) of plant powder.
Determination of TPC
The TPC of the prepared extracts was determined using the colorimetric Folin-Ciocalteu method (Jung et al., 2008). The calibration curve was constructed using gallic acid as standard at a concentration range of 0 to 20 mg/L, showing a linear equation of
Antioxidant activities
where A is the absorbance of the test sample, and B is the absorbance of the blank sample.
The half-maximal inhibitory concentration (IC50) was calculated from the mean values of three measurements at the used concentration range. Gallic acid was used as a positive control with the IC50 of 5.62 μg/mL.
Evaluation of melanosis formation and lipid peroxidation inhibition in shrimp
where C is the actual gray value of the shrimp sample, and D is the average gray value of the shrimp on the first day.
Analysis method
RESULTS AND DISCUSSION
Total phenolic content
Fig. 1 shows the TPC of the prepared extracts. All extracts had high TPC with values ranging between 44.5±1.1 [‘034’ seed (OS)] and 144.7±1.9 mg GAE/g DW [‘Nuoc’ peel (NP)] (
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Figure 1. Total phenolic content (TPC) of 9 avocado by-product extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)]. Values represent the mean±standard deviation (n=3). Different letters (a-f) indicate significant differences (
P <0.05).
Melanosis evaluation
Fig. 2 shows the melanosis scores in shrimp carapace treated with avocado by-product extracts (0.025%, w/v), SMS (1.25%, w/v), and the control (with water) during 8 days storage at 4°C. Changes in mean gray value were the indication of melanosis. It is also worth noting that high melanosis prevention level was associated with low decreasing level in mean gray value during storage. At day 0, there were no significant differences in the gray values (
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Figure 2. Changes in mean gray values of the carapace area of whiteleg shrimp,
Litopenaus vannamei treated with different extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)] during refrigerated storage, compared with that of sodium metabisulfite (SMS) and the control. Different uppercase letters (A-D) are related to significant differences among other storage days in the same treatment (P <0.05). Different lowercase letters (a-g) showed significant differences among other treatments in the same storage time (P <0.05).
Lipid peroxidation inhibition
Fig. 3 shows changes in TBARS values of whiteleg shrimp treated with the prepared extracts (0.025%, w/v), SMS (1.25%, w/v), and control (deionized water). No significant difference was observed in TBARS values among all samples at day 0 (
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Figure 3. Changes in TBARS values of whiteleg shrimp,
Litopenaus vannamei treated with different extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)] during refrigerated storage, compared with that of sodium metabisulfite (SMS) and the control. Different uppercase letters (A-E) are related to significant differences among other storage days in the same treatment (P <0.05). Different lowercase letters (a-h) showed significant differences among other treatments in the same storage time (P <0.05).
Antioxidant activities
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Figure 4. DPPH radical inhibitory activity of 9 avocado by-product extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)]. Different uppercase letters (A-E) are related to significant differences among other storage days in the same treatment (
P <0.05). Different lowercase letters (a-f) showed significant differences among other treatments in the same storage time (P <0.05).
At the highest concentration of 100 μg/mL, the prepared extracts displayed DPPH scavenging percentage between 73.4±1.0 and 99.0±0.5% and IC50 values of 3.6 to 63.1 μg/mL. It is noted that the scavenging activity of avocado by-products in this study was significantly higher than those of avocado peels and seeds in previous studies. Melgar et al. (2018) showed that IC50 values calculated from a DPPH radical scavenging assay for the hydroethanolic extracts of
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Figure 5. Reducing power of 9 avocado by-product extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)]. Different uppercase letters (A-C) are related to significant differences among other storage days in the same treatment (
P <0.05). Different lowercase letters (a-f) showed significant differences among other treatments in the same storage time (P <0.05).
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Figure 6. Tyrosinase inhibitory activity of 9 avocado by-product extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)]. Different uppercase letters (A-E) are related to significant differences among other storage days in the same treatment (
P <0.05). Different lowercase letters (a-h) showed significant differences among other treatments in the same storage time (P <0.05).
Melanosis in shrimp was characterized by the formation of black spots caused by the oxidation of phenol substrates (such as tyrosine) to quinones catalyzed by polyphenoloxidase (Gonçalves and de Oliveira, 2016; Pan et al., 2019). Phenolic compounds could alleviate melanosis formation in different mechanisms based on the elimination of one or more important components involved in the enzymatic reaction, such as oxygen, copper, substrate, and the enzyme itself. Certain polyphenols can lower PPO activity by direct interaction with PPO through chelating or forming hydrogen bonding and evenly donating an electron to the intermediate quinones, and hence they could interrupt the oxidation process (Sae-leaw and Benjakul, 2019). Several polyphenols have been documented with intense PPO inhibitory activity such as catechin and its derivatives, quercetin and its derivatives, and coumaric acid (Sae-leaw et al., 2017; Rosero et al., 2019). Among various polyphenolic compounds found in avocado by-products, 30 of them belonged to organic acids, hydroxycinnamic acids, catechins, free and glycosylated flavonoids, and dimeric and trimeric procyanidins. Catechin, epicatechin, six quercetin derivatives, four dimeric procyanidins, and three trimeric procyanidins were identified in the most active fractions of avocado peel and seeds reported in the literature (Rosero et al., 2019). Catechin and its derivatives exhibited tyrosinase inhibitory activity based on the combined effects of metal chelation and the reduction of quinone (Nirmal and Benjakul, 2012). As shown in Fig. 1 the prepared extracts of avocado by-products were rich in polyphenols, which could explain the significant retardation of melanosis formation in shrimp during storage.
Fig. 7 plots the correlations of the anti-melanosis of the prepared extracts to their TPC values, the oxidant inhibitory activities and lipid peroxidation (TBARS) values at day 6 storage (confidence level of 95%). The data at the 6th day was chosen because it showed the most variation in the melanosis score (Fig. 2). It is clearly seen that the melanosis inhibition on shrimp stored up to 6 days had a good correlation with the TPC and antioxidant activities of the corresponding extracts (r=0.547∼0.857). The high correlation coefficient r of 0.811 for the TPC value could confirm the important role of phenolic compounds in the prepared by-product extracts on retarding melanosis formation in shrimp. It should be noted that the scavenging activity toward DPPH radical behaved in the same manner with TPC value toward melanosis inhibitory activity as the DPPH scavenging activity (r=0.857) was known to be consistent with the TPC value (Sun et al., 2014; Sae-leaw and Benjakul, 2019; Shiekh et al., 2019). A moderate correlation with tyrosinase inhibitory activity (r=0.588) indicates that tyrosinase, a common enzyme found in crustaceans, also plays a reasonable role in melanosis formation. The lower Pearson coefficient (r) for tyrosinase inhibition than TPC value could be explained through different melanosis-inhibition mechanisms during cold storage of shrimp with avocado by-product extracts. A similar relationship was found for the FRAP data. However, the values for TBARS indicated the decrease in quality of shrimp, which was due to the formation of lipid oxidizing products (e.g., aldehydes produce off flavors) (Chaijan et al., 2006; Zhang et al., 2015) This high absolute r value indicated that retardation of both melanosis and lipid peroxidation were attributed to the high phenolic content in the extracts. Phenolic compounds might chelate the metal pro-oxidants in shrimp muscle and that resulted in the delay of lipid oxidation in shrimp (Abbasvali et al., 2016). Sai-Ut et al. (2020) reported that extract of mango seed kernel possessing rich phenolic compounds could appreciably retard the melanosis formation and lipid oxidation process. Further studies on the influence of phenolic profiles on melanosis prevention and lipid oxidation inhibition should be investigated.
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Figure 7. Pearson’s correlation coefficient (r) of the melanosis inhibitory activity (at day 6 storage) to total phenolic content (TPC), antioxidant activities (DPPH radical scavenging, ferric reducing power (FRAP) and tyrosinase enzyme inhibition (at concentration of 100 μg/mL), and TBARS.
Overall, the present study highlights the promising applications of avocado by-product (seed and peel) extracts as efficient inhibitors of black spots and lipid oxidation during refrigerated storage of whiteleg shrimp. These inhibitory activities varied depending on the type of avocado fruits, which was due to the difference in TPC and antioxidant power among them. Between the investigated samples, the extract of ‘Nuoc’ avocado peel showed the most promising impact for shrimp preservation with its high TPC (144.7±1.9 mg GAE/g DW) and antioxidant activities (IC50 values for DPPH and PPO inhibition assays of 2.3 and 48.0 μg/mL, respectively). These properties were even better than those of the commercial SMS additive at high preserving dose. Therefore, these avocado by-products can be considered as safe and cheap natural sources of bioactive compounds for anti-melanosis and extending shelf life of whiteleg shrimp, contributing to environmental pollution prevention and added economic value.
ACKNOWLEDGEMENTS
This work belongs to the project grant 67/2019/HĐ-QPTKHCN funded by Ho Chi Minh City Department of Science and Technology, Viet Nam. The study was supported by Ho Chi Minh City University of Technology and Education, Viet Nam.
AUTHOR DISCLOSURE STATEMENT
The authors declare no conflict of interest.
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Article
Original
Prev Nutr Food Sci 2021; 26(2): 209-218
Published online June 30, 2021 https://doi.org/10.3746/pnf.2021.26.2.209
Copyright © The Korean Society of Food Science and Nutrition.
Inhibition of Melanosis in Whiteleg Shrimp (Litopenaeus vannamei) during Refrigerated Storage Using Extracts of Different Avocado (Persea americana Mill.) By-Products
Dao Thi Anh Phan1 , Trung Huu Bui1, Tram Quynh Thi Doan1, Nguyen Van Nguyen2, and Trieu Hai Ly3
1Faculty of Chemical and Food Technology, HCMC University of Technology and Education, Ho Chi Minh 70000, Viet Nam
2Research Center for Aquafeed Nutrition and Fishery Post-Harvest Technology (APOTEC), Ho Chi Minh 70000, Viet Nam
3Research Center of Ginseng and Medicinal Materials, National Institute of Medicinal Materials, Ho Chi Minh 70000, Viet Nam
Correspondence to:Phan Thi Anh Dao, Tel: +84-902-373-656, E-mail: daopta@hcmute.edu.vn
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Abstract
Melanosis in shrimp usually leads to reduction in its shelf life and quality, which causes a significant loss in economic value of shrimp products. This study reports potential applications of nine ethanolic extracts of by-products, i.e., peel and/or seed from three Vietnamese avocado varieties as effective inhibitors of melanosis in whiteleg shrimp. Six out of nine shrimp samples treated with the prepared extracts (0.025%, w/v) reduced melanosis and lipid oxidation more significantly as compared to those treated with sodium metabisulfite (SMS, 1.25%, w/v) and control groups (treated with water) during 8-day storage at 4°C (P<0.05). These six extracts had mean gray values ranging from 47.0±0.7 to 57.3±0.4% were lower than those treated with SMS (mean gray of 39.8±0.4%). The inhibition of melanosis and lipid oxidation in shrimp for these extracts could be attributed to their high content of polyphenols [total phenolic content (TPC) from 44.5±1.1 to 144.7±1.9 mg gallic acid equivalents/g dried weight] and strong antioxidant activities [including 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging, ferric reducing antioxidant power (FRAP), and tyrosinase enzyme inhibition]. Pearson statistical analysis showed strong correlation for melanosis inhibition to TPC and DPPH scavenging (r>0.80) followed by tyrosinase inhibition and FRAP (r>0.50). The findings obtained from this study suggest potential utilization of avocado by-product extracts as safe and cheap natural alternatives to traditional sulfites for anti-melanosis and shelf life extension of whiteleg shrimp.
Keywords: antioxidant, avocado by-products, melanosis, tyrosinase, whiteleg shrimp
INTRODUCTION
Whiteleg shrimp (
Melanosis in shrimp and other crustaceans is developed by the oxidation of phenol substrates (such as tyrosine in shrimp) to quinones catalyzed by polyphenolase, which generates dark pigments of high molecular compounds (Sae-leaw and Benjakul, 2019). From a commercial perspective, some methods have been used to prevent melanosis development in shrimp during storage, such as treatments with sulfite and phosphate compounds (Martínez-Álvarez et al., 2008; Galvão et al., 2017). However, the potential risks of using those chemical additives, i.e., nausea, abdominal pain, vomiting, and choking have raised awareness among customers and regulators. Consequently, researchers and scientists worldwide have recently paid considerable attention to natural, safe, and effective additives (Djeridane et al., 2006; Encarnacion et al., 2012). Natural antioxidant substances have been widely studied as substitutes to chemical additives to prevent melanosis. Natural additives, such as tocopherols, flavonoids, cinnamic acids, and coumarins were reported to exhibit potent antioxidant, antimicrobial, and polyphenoloxidase (PPO) inhibitory activities and thus, they could prevent the melanosis process (Gonçalves and de Oliveira, 2016). Plant extracts containing polyphenolic compounds demonstrated a significant retardation of melanosis formation in crustaceans, which was associated with tyrosinase inhibitory activity (Sae-leaw and Benjakul, 2019). Nirmal and Benjakul (2012) reported that the ethanolic extract of green tea containing a high amount of catechin and derivatives could significantly decrease the lipid oxidation and melanosis formation in whiteleg shrimp during cold storage. Encarnacion et al. (2012) prepared an extract of edible mushroom (
Recently, studies on utilizing agricultural by-products for food additives and preservation have been extensively investigated due to economic and environmental benefits (Gómez et al., 2014; Saavedra et al., 2017). Among various by-products, avocado seed and peel contained great amounts of phenolic compounds, including flavanol monomers, proanthocyanidins, hydroxycinnamic acids, and flavonol glycosides (Kosińska et al., 2012). This would attribute to a high potential of antioxidant activities of those by-products. Rodríguez-Carpena et al. (2011) showed that raw porcine patties treated with the extracts of avocado peel and seed could effectively inhibit lipid oxidation and color deterioration during chilled storage. Several studies also reported the applications of avocado by-products as potential sources of natural antioxidants or preservatives (Gómez et al., 2014: Saavedra et al., 2017; Gashahun and Solomon, 2018).
It is worth mentioning that avocado peel and seed are discarded as wastes, accounting for about 20% (w/w) of the fruit (Wang et al., 2010). Avocados are widely grown in Viet Nam, which has been considered as one of the seven important fruits crops in the country. Consequently, a large quantity of avocado by-products is discarded from fruit processing annually. Although the phenolic compounds, such as catechin, quercetin, and their derivatives from avocado by-products could exhibit a potential in preventing melanosis on crustaceans or shrimps (Nirmal and Benjakul, 2012; Qian et al., 2018; Tremocoldi et al., 2018; Rosero et al., 2019), to the best of our knowledge, there has been no report on utilizing avocado by-products as potential natural additives to prevent melanosis and/or extend the shelf life of whiteleg shrimp.
In this study, the roles of some popular avocado by-products on the retardation of melanosis and lipid oxidation in whiteleg shrimp during cold storage were evaluated and discussed. The study aimed to obtain three main objectives: (i) preparation of nine ethanolic extracts from by-products (seeds and peels) of three avocado varieties from Viet Nam, and determination of their total phenolic content (TPC) and antioxidant activities; (ii) evaluation of the capability of these prepared extracts in preventing melanosis formation and lipid oxidation in whiteleg shrimp during 8 days storage at 4°C; and (iii) discussion on the relationship between the inhibition on melanosis of these prepared extracts and their TPC values and antioxidant activities. The utilization of these by-products as food additives could not only reduce the negative impact on the environment but also expand the range of avocado value-added products.
MATERIALS AND METHODS
Materials and chemicals
Folin-Ciocalteu reagent, iron (III) chloride hexahydrate (FeCl3・6H2O), malondialdehyde (MDA), sodium metabisulfite (SMS), potassium hexacyanoferrate [K3Fe(CN)6], thiobarbituric acid (TBA), trichloracetic acid (TCA), gallic acid, kojic acid, 2,2-diphenyl-1-picrylhydrazyl (DPPH), and tyrosinase were purchased from Sigma-Aldrich Co. (St. Louis, MO, USA). All other chemicals were of analytical grade.
By-products (peels and seeds) from three popular varieties of avocado, namely ‘Nuoc’, ‘Sap’, and ‘034’ were supplied from several local markets in Ho Chi Minh City, Viet Nam. The samples were then dried to the moisture content of about 10% [using a gravimetric method followed by the European Brewery Convention (2000)]. The dried samples were subsequently ground in a blender into a homogenous fine pulp that was then extracted with ethanol.
Alive whiteleg shrimp with the size of 30∼40 shrimps/kg were purchased from Tan Binh market (Ho Chi Minh City, Viet Nam). The shrimps were immediately transported to the laboratory for the experiments.
Preparation of extracts
An extract of each avocado by-product was prepared using a maceration technique (Azwanida, 2015). Dried powder (30 g) was soaked in 100 mL of 70% ethanol (v/v) at 32°C for 24 h. The mixture was filtered to collect the extract solution, and the remaining residue was re-extracted with ethanol twice using the same procedure. Then, the mixture of three collected extracts was concentrated using a rotary evaporator to produce a crude extract. Table 1 presents the extraction yield (E%) of the nine prepared avocado by-product extracts. It includes three seed extracts and three peel extracts prepared from each variety [‘Sap’, ‘034’, and ‘Nuoc’: No. (1) to (6)], and three mixed extracts [No. (7) to (9)] consisting of peel mixture, seed mixture, and peel-seed mixture from 3 varieties mixed in equal weights. Note, the extraction yield (E%) can be calculated as in Eq. (1):
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Table 1 . The extraction yield of nine extracts prepared from by-products of three avocado varieties: ‘Sap’, ‘034’, ‘Nuoc’.
No. Sample name Formulation/mixture Extraction yield (%) 1 SS Sap seed 12.5 2 SP Sap peel 10.0 3 OS 034 seed 10.1 4 OP 034 peel 7.6 5 NS Nuoc seed 18.1 6 NP Nuoc peel 7.8 7 MS Sap seed+034 seed+Nuoc seed 13.5 8 MP Sap peel+034 peel+Nuoc peel 7.6 9 MSP Mixture of all seeds and peels 9.8
where mextract is the weight (g) of the dried extract residue obtained after solvent removal, and mpowder is the weight (g) of plant powder.
Determination of TPC
The TPC of the prepared extracts was determined using the colorimetric Folin-Ciocalteu method (Jung et al., 2008). The calibration curve was constructed using gallic acid as standard at a concentration range of 0 to 20 mg/L, showing a linear equation of
Antioxidant activities
where A is the absorbance of the test sample, and B is the absorbance of the blank sample.
The half-maximal inhibitory concentration (IC50) was calculated from the mean values of three measurements at the used concentration range. Gallic acid was used as a positive control with the IC50 of 5.62 μg/mL.
Evaluation of melanosis formation and lipid peroxidation inhibition in shrimp
where C is the actual gray value of the shrimp sample, and D is the average gray value of the shrimp on the first day.
Analysis method
RESULTS AND DISCUSSION
Total phenolic content
Fig. 1 shows the TPC of the prepared extracts. All extracts had high TPC with values ranging between 44.5±1.1 [‘034’ seed (OS)] and 144.7±1.9 mg GAE/g DW [‘Nuoc’ peel (NP)] (
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Figure 1. Total phenolic content (TPC) of 9 avocado by-product extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)]. Values represent the mean±standard deviation (n=3). Different letters (a-f) indicate significant differences (
P <0.05).
Melanosis evaluation
Fig. 2 shows the melanosis scores in shrimp carapace treated with avocado by-product extracts (0.025%, w/v), SMS (1.25%, w/v), and the control (with water) during 8 days storage at 4°C. Changes in mean gray value were the indication of melanosis. It is also worth noting that high melanosis prevention level was associated with low decreasing level in mean gray value during storage. At day 0, there were no significant differences in the gray values (
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Figure 2. Changes in mean gray values of the carapace area of whiteleg shrimp,
Litopenaus vannamei treated with different extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)] during refrigerated storage, compared with that of sodium metabisulfite (SMS) and the control. Different uppercase letters (A-D) are related to significant differences among other storage days in the same treatment (P <0.05). Different lowercase letters (a-g) showed significant differences among other treatments in the same storage time (P <0.05).
Lipid peroxidation inhibition
Fig. 3 shows changes in TBARS values of whiteleg shrimp treated with the prepared extracts (0.025%, w/v), SMS (1.25%, w/v), and control (deionized water). No significant difference was observed in TBARS values among all samples at day 0 (
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Figure 3. Changes in TBARS values of whiteleg shrimp,
Litopenaus vannamei treated with different extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)] during refrigerated storage, compared with that of sodium metabisulfite (SMS) and the control. Different uppercase letters (A-E) are related to significant differences among other storage days in the same treatment (P <0.05). Different lowercase letters (a-h) showed significant differences among other treatments in the same storage time (P <0.05).
Antioxidant activities
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Figure 4. DPPH radical inhibitory activity of 9 avocado by-product extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)]. Different uppercase letters (A-E) are related to significant differences among other storage days in the same treatment (
P <0.05). Different lowercase letters (a-f) showed significant differences among other treatments in the same storage time (P <0.05).
At the highest concentration of 100 μg/mL, the prepared extracts displayed DPPH scavenging percentage between 73.4±1.0 and 99.0±0.5% and IC50 values of 3.6 to 63.1 μg/mL. It is noted that the scavenging activity of avocado by-products in this study was significantly higher than those of avocado peels and seeds in previous studies. Melgar et al. (2018) showed that IC50 values calculated from a DPPH radical scavenging assay for the hydroethanolic extracts of
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Figure 5. Reducing power of 9 avocado by-product extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)]. Different uppercase letters (A-C) are related to significant differences among other storage days in the same treatment (
P <0.05). Different lowercase letters (a-f) showed significant differences among other treatments in the same storage time (P <0.05).
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Figure 6. Tyrosinase inhibitory activity of 9 avocado by-product extracts [Sap seed (SS), Sap peel (SP), 034 seed (OS), 034 peel (OP), Nuoc seed (NS), Nuoc peel (NP), seed mixture (MS), peel mixture (MP), and peel and seed mixture (MSP)]. Different uppercase letters (A-E) are related to significant differences among other storage days in the same treatment (
P <0.05). Different lowercase letters (a-h) showed significant differences among other treatments in the same storage time (P <0.05).
Melanosis in shrimp was characterized by the formation of black spots caused by the oxidation of phenol substrates (such as tyrosine) to quinones catalyzed by polyphenoloxidase (Gonçalves and de Oliveira, 2016; Pan et al., 2019). Phenolic compounds could alleviate melanosis formation in different mechanisms based on the elimination of one or more important components involved in the enzymatic reaction, such as oxygen, copper, substrate, and the enzyme itself. Certain polyphenols can lower PPO activity by direct interaction with PPO through chelating or forming hydrogen bonding and evenly donating an electron to the intermediate quinones, and hence they could interrupt the oxidation process (Sae-leaw and Benjakul, 2019). Several polyphenols have been documented with intense PPO inhibitory activity such as catechin and its derivatives, quercetin and its derivatives, and coumaric acid (Sae-leaw et al., 2017; Rosero et al., 2019). Among various polyphenolic compounds found in avocado by-products, 30 of them belonged to organic acids, hydroxycinnamic acids, catechins, free and glycosylated flavonoids, and dimeric and trimeric procyanidins. Catechin, epicatechin, six quercetin derivatives, four dimeric procyanidins, and three trimeric procyanidins were identified in the most active fractions of avocado peel and seeds reported in the literature (Rosero et al., 2019). Catechin and its derivatives exhibited tyrosinase inhibitory activity based on the combined effects of metal chelation and the reduction of quinone (Nirmal and Benjakul, 2012). As shown in Fig. 1 the prepared extracts of avocado by-products were rich in polyphenols, which could explain the significant retardation of melanosis formation in shrimp during storage.
Fig. 7 plots the correlations of the anti-melanosis of the prepared extracts to their TPC values, the oxidant inhibitory activities and lipid peroxidation (TBARS) values at day 6 storage (confidence level of 95%). The data at the 6th day was chosen because it showed the most variation in the melanosis score (Fig. 2). It is clearly seen that the melanosis inhibition on shrimp stored up to 6 days had a good correlation with the TPC and antioxidant activities of the corresponding extracts (r=0.547∼0.857). The high correlation coefficient r of 0.811 for the TPC value could confirm the important role of phenolic compounds in the prepared by-product extracts on retarding melanosis formation in shrimp. It should be noted that the scavenging activity toward DPPH radical behaved in the same manner with TPC value toward melanosis inhibitory activity as the DPPH scavenging activity (r=0.857) was known to be consistent with the TPC value (Sun et al., 2014; Sae-leaw and Benjakul, 2019; Shiekh et al., 2019). A moderate correlation with tyrosinase inhibitory activity (r=0.588) indicates that tyrosinase, a common enzyme found in crustaceans, also plays a reasonable role in melanosis formation. The lower Pearson coefficient (r) for tyrosinase inhibition than TPC value could be explained through different melanosis-inhibition mechanisms during cold storage of shrimp with avocado by-product extracts. A similar relationship was found for the FRAP data. However, the values for TBARS indicated the decrease in quality of shrimp, which was due to the formation of lipid oxidizing products (e.g., aldehydes produce off flavors) (Chaijan et al., 2006; Zhang et al., 2015) This high absolute r value indicated that retardation of both melanosis and lipid peroxidation were attributed to the high phenolic content in the extracts. Phenolic compounds might chelate the metal pro-oxidants in shrimp muscle and that resulted in the delay of lipid oxidation in shrimp (Abbasvali et al., 2016). Sai-Ut et al. (2020) reported that extract of mango seed kernel possessing rich phenolic compounds could appreciably retard the melanosis formation and lipid oxidation process. Further studies on the influence of phenolic profiles on melanosis prevention and lipid oxidation inhibition should be investigated.
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Figure 7. Pearson’s correlation coefficient (r) of the melanosis inhibitory activity (at day 6 storage) to total phenolic content (TPC), antioxidant activities (DPPH radical scavenging, ferric reducing power (FRAP) and tyrosinase enzyme inhibition (at concentration of 100 μg/mL), and TBARS.
Overall, the present study highlights the promising applications of avocado by-product (seed and peel) extracts as efficient inhibitors of black spots and lipid oxidation during refrigerated storage of whiteleg shrimp. These inhibitory activities varied depending on the type of avocado fruits, which was due to the difference in TPC and antioxidant power among them. Between the investigated samples, the extract of ‘Nuoc’ avocado peel showed the most promising impact for shrimp preservation with its high TPC (144.7±1.9 mg GAE/g DW) and antioxidant activities (IC50 values for DPPH and PPO inhibition assays of 2.3 and 48.0 μg/mL, respectively). These properties were even better than those of the commercial SMS additive at high preserving dose. Therefore, these avocado by-products can be considered as safe and cheap natural sources of bioactive compounds for anti-melanosis and extending shelf life of whiteleg shrimp, contributing to environmental pollution prevention and added economic value.
ACKNOWLEDGEMENTS
This work belongs to the project grant 67/2019/HĐ-QPTKHCN funded by Ho Chi Minh City Department of Science and Technology, Viet Nam. The study was supported by Ho Chi Minh City University of Technology and Education, Viet Nam.
AUTHOR DISCLOSURE STATEMENT
The authors declare no conflict of interest.
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Table 1 . The extraction yield of nine extracts prepared from by-products of three avocado varieties: ‘Sap’, ‘034’, ‘Nuoc’
No. Sample name Formulation/mixture Extraction yield (%) 1 SS Sap seed 12.5 2 SP Sap peel 10.0 3 OS 034 seed 10.1 4 OP 034 peel 7.6 5 NS Nuoc seed 18.1 6 NP Nuoc peel 7.8 7 MS Sap seed+034 seed+Nuoc seed 13.5 8 MP Sap peel+034 peel+Nuoc peel 7.6 9 MSP Mixture of all seeds and peels 9.8
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