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| ORIGINAL ARTICLE |
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| Year : 2018 | Volume
: 11
| Issue : 12 | Page : 676-681 |
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Ultrasound-assisted extraction of antioxidant polyphenolic compounds from Nephelium lappaceum L. (Mexican variety) husk
Adriana Mendez-Flores1, Ayerim Hérnandez-Almanza1, Aidé Sáenz-Galindo2, Jesús Morlett-Chávez3, Cristóbal N Aguilar1, Juan Ascacio-Valdés1
1 Bioprocesses and Bioproducts Research Group, Food Research Department, School of Chemistry, Autonomous University of Coahuila, Blvd. Venustiano Carranza, Col. República, Saltillo, 25280, Coahuila, México
2 Organic Chemistry Department, School of Chemistry, Autonomous University of Coahuila, Blvd. Venustiano Carranza, Col. República, Saltillo, 25280, Coahuila, México
3 Molecular Biology Laboratory, School of Chemistry, Autonomous University of Coahuila, Blvd. Venustiano Carranza, Col. República, Saltillo, 25280, Coahuila, México
| Date of Submission | 28-May-2018 |
| Date of Decision | 30-Aug-2018 |
| Date of Acceptance | 20-Oct-2018 |
| Date of Web Publication | 26-Dec-2018 |
Correspondence Address:
Juan Ascacio-Valdés
Bioprocesses and Bioproducts Research Group, Food Research Department, School of Chemistry, Autonomous University of Coahuila, Blvd. Venustiano Carranza, Col. República, Saltillo, 25280, Coahuila
México
 Source of Support: None, Conflict of Interest: None  | 17 |
DOI: 10.4103/1995-7645.248339
Objective: To reach the recovery and identification of antioxidant polyphenolic compounds from Nephelium lappaceum L. (Mexican variety) husk using ultrasound-assisted extraction and liquid chromatography/mass spectrometry as well as the in vitro antioxidant activity. Methods: Rambutan husk extracts were obtained by ultrasound-assisted extraction, mass/ volume ratio, water/ethanol percentage and extraction time were evaluated. Once the best extraction condition of polyphenolic compounds was defined, a polyphenolic fraction was recovered using Ambetlite XAD-16. The total content of antioxidant polyphenolic compounds was determined by summation of the total hydrolysable polyphenol and total condensed polyphenol contents. Recovered compounds were identified by FTIR (ATR) spectroscopy and HPLC/ESI/MS. The antioxidant activity was carried out by ABTS, DPPH and lipid oxidation inhibition in vitro methods. Results: In Mexican variety rambutan husk, the total polyphenolic content was 487.67 mg/g, after ultrasound-assisted extraction. According to the HPLC/ESI/MS analysis 12 antioxidant polyphenolic compounds were identified, mostly ellagitannins such as geraniin, corilagin and ellagic acid. The antioxidant activity determined by ABTS, DPPH and lipid oxidation inhibition methods was demonstrated. The main functional groups of the identified compounds were determined by FTIR analysis. Conclusions: It was demonstrated that ultrasound-assisted extraction was effective and allowed the extraction and recovery of antioxidant polyphenolic compounds. Furthermore Mexican variety rambutan husk is an important source for recovering polyphenolic compounds with antioxidant activity, these compounds have potential application for the treatment/prevention of various diseases related to cancer and pathogenic microorganisms. Keywords: Mexican variety rambutan, Ultra-sound assisted extraction, Antioxidant polyphenolic compounds, HPLC/ESI/MS
How to cite this article:
Mendez-Flores A, Hérnandez-Almanza A, Sáenz-Galindo A, Morlett-Chávez J, Aguilar CN, Ascacio-Valdés J. Ultrasound-assisted extraction of antioxidant polyphenolic compounds from Nephelium lappaceum L. (Mexican variety) husk. Asian Pac J Trop Med 2018;11:676-81 |
How to cite this URL:
Mendez-Flores A, Hérnandez-Almanza A, Sáenz-Galindo A, Morlett-Chávez J, Aguilar CN, Ascacio-Valdés J. Ultrasound-assisted extraction of antioxidant polyphenolic compounds from Nephelium lappaceum L. (Mexican variety) husk. Asian Pac J Trop Med [serial online] 2018 [cited 2023 Apr 2];11:676-81. Available from: https://www.apjtm.org/text.asp?2018/11/12/676/248339 |
| 1. Introduction | |  |
Phenolic compounds constitute a wide group of chemical substances, are produced by plant secondary metabolism and are considered bioactive compounds[1]. Their biological properties give the bioactive activity, the interest for new medicine/supplements and high added value compounds[2]. Principal biological properties are antimicrobial activity[3],[4], antidiabetic[5],[6], anticancer[7], antiparasitic[8], among others. Polyphenols are present in different plants species, one of these with high phenolic content and few applications in the industry is the rambutan (Nephelium lappaceum L.). Rambutan is a red or yellow ovoid Malaysian tropical fruit, member from the Sapindaceae family[9], its husk represents 45.7% of its total weight[10] and is currently cultivated in some places of India, Indonesia, Thailand, Costa Rica, Guatemala and Mexico[11]. Rambutan varieties native from Malaysia and Indonesia were introduced to Mexico in the 1950s, the crop started in Chiapas and later was spread to other states (as Veracruz, Tabasco, among others)[11]. In Mexico, the pulp is the principal commercialized part of the fruit, it is consumed in fresh or it is used to obtain some processed products[12], however, this practice generates important quantities of not used wastes. Some reports declare that the rambutan husk contains phenolic compounds with different chemical structures and they are considered as bioactive. Other reports mentioned that rambutan husk polyphenols has antioxidant capacity, which are able to inhibit free radicals responsible of cellular oxidation[13]; inhibit the pathogenic bacteria Streptococcus pyogenes, Staphylococcus aureus and Pseudomonas aeruginosa growth for mention some examples[14]; has antidiabetic activity by reducing the cholesterol and triglycerides blood concentrations and glycosylated serum protein[15]. Other studies demonstrated the cytotoxic effects of bioactive compounds against 4T1 breast cancer cells and mouse embryonic fibroblasts cells[16], inhibition of the human immunodeficiency virus (HIV) replication and antiparasitic activity against Trypanosoma cruzi, Leishmania infantum, among others.
Despite the multiple applications there are few reports about the extraction and identification of phenolic compounds present in Mexican variety rambutan husk, this subject is crucial to develop different extraction strategies that assure the bioactivity for these high added value compounds. The objective of this study was the recovery by ultrasound-assisted extraction of antioxidant polyphenolic compounds from Mexican variety rambutan husk, the identification of the recovered compounds by liquid chromatography/ mass spectrometry and to determinate its antioxidant activity in vitro.
| 2. Materials and methods | | |
2.1. Plan material
The Mexican variety rambutan husks (Soconusco region, Comitán, Chiapas, Mexico) were dehydrated at 50 °C for 48 h in a conventional oven[10], then was processed in a blade mill.
2.2 Extraction and purificaction of rambutan husk polyphenols
In order to define the best extraction condition of total polyphenolic compounds, experiments were performed under a completely randomized experimental design with factorial arrangement by ultrasound-assisted extraction; ANOVA and Duncan’s test were done and all experiments were carried out by triplicate. Evaluated factors were mass/volume ratio (g/mL), ultrasound extraction time (min) and ethanol/water percentage (extractor agent), all experiments were performed at room temperature. [Table 1] described the evaluated extraction conditions and the samples ID. With the best extraction condition identified, obtained extract was processed by liquid column chromatography with Amberlite XAD-16 to recover a polyphenolic fraction. Ethanol was evaporated and the polyphenols were recovered as a fine powder.
2.3. Determination of total hydrolysable polyphenols
Total hydrolysable polyphenols were determined using Folin’s Ciocaulteu reagent[10]. Experiment was performed by triplicate, total hydrolysable polyphenols content was expressed as gallic acid equivalents (GAE).
2.4. Determination of total condensed polyphenols
Total condensed polyphenols were quantified using ferric reagent and HCl-butanol[10]. The experiment was performed by triplicate, total condensed polyphenols concentration was expressed as catechin equivalents.
2.5. ABTS antioxidant assay
For the formation of ABTS.+ radical, 2.45 mM potassium persulfate was mixed with 7 mM ABTS solution (1:2 v/v). The mixture was carried out and rest in the dark at room temperature for 12-16 h. Subsequently, absorbance was measured at 734 nm, the solution was diluted with ethanol until (0.70±0.02) absorbance. For this study, 10 μL of sample (rambutan husk polyphenols) were mixed with 1 mL of ABTS adjusted solution and the absorbance was measured. Water was used as control and the results were reported by inhibition percentage (all experiments were carried out by triplicate).
A= absorbance (nm)
2.6. DPPH antioxidant assay
The 2,2-diphenyl-1-picrylhydracyl (DPPH) free radical scavenging was quantified as follows. Briefly, DPPH (Sigma Aldrich Mexico ®) was prepared at 60 μM concentration in absolute methanol. Subsequently,193 μL of DPPH-methanol solution were mixed with 7 μL of sample (rambutan husk polyphenols), the solution was allowed to stand for 30 min at room temperature, then the absorbance of solutions was determined by micro-plate reader (TECAN®Sunrise) at 517 nm. DPPH-methanol was used as a control. And the results were reported as inhibition percentage using the above mentioned equation (all experiments were carried out by triplicate).
2.7. Lipid oxidation inhibition (LOI) assay
For the assay, linoleic acid was employed as the lipid source. Linoleic acid solution was prepared with 0.35 g of linoleic acid and 0.937 g of Tween 20 in 5 mL of 96% ethanol. A total of 50 μL of sample (rambutan husk polyphenols) was mixed with 100 μL linoleic acid solution and 1.5 mL of 0.02 M acetate buffer pH 4.0.The mixture was homogenized and then incubated for 1 min at 37 °C Immediately, 750 μL of 0.5 mM FeCl2-EDTA were added to induce the oxidation and the samples were incubated for 1 and 24 h at 37 °C After each incubation time, 250 μL of solution was mixed with 1mL 0.1 M NaOH in 10% ethanol. Subsequently, 2.5 mL of 10% ethanol was added and the absorbance was measured at 232 nm,10% ethanol was used as blank. Antioxidant activity percentage was calculated using the equation:
where: ΔDcontrol is the difference between the absorbance of the control (distilled water) after 24 h and 1 h of incubation, and Δ Dsample is the difference between the absorbance of the sample after 24 and 1 h of incubation (all experiments were carried out by triplicate).
2.8. FTIR analysis
Polyphenol powder recovered after Ambertilte XAD-16 chromatography was placed on a metal plate to carry out the spectrophotometric analysis in a Perkin Elmer Spectrum FTIR model 65, using 16 sweeps as operation condition.
2.9. Identification of polyphenolic compounds by HPLC/ESI/MS analysis
The analysis by high performance liquid chromatography (HPLC) was performed on a Varian HPLC system including an autosampler (VarianProStar 410, USA), a ternary pump (VarianProStar 230I, USA) and a PDA detector (VarianProStar 330, USA). A liquid chromatograph ion trap mass spectrometer (Varian 500-MS IT Mass Spectrometer, USA) equipped with an electrospray ion source was used. Samples (5 μL) were injected into a Denali C18 column (150 mm × 2.1 mm, 3 μm, Grace, USA). The oven temperature was maintained at 30 The eluents were formic acid (0.2 %, v/v; solvent A) and acetonitrile (solvent B). Applied gradient was: initial, 3% B; 0–5 min, 9% B linear; 5–15 min, 16% B linear; 15–45 min, 50% B linear. The column was washed and reconditioned. The flow rate was maintained at 0.2 mL/min and elution was monitored at 245, 280, 320 and 550 nm. The whole effluent (0.2 mL/min) was injected into the source of the mass spectrometer, without splitting. All MS experiments were performed in the negative mode [M-H]-1. Nitrogen was used as nebulizing gas and helium as damping gas. The ion source parameters were: spray voltage 5.0 kV and, capillary voltage and temperature were 90.0 V and 350 respectively. Data were collected and processed using MS Workstation software (V 6.9). Samples were firstly analyzed in full scan mode acquired in the m/z range 50–2 000. MS/MS analyses were performed on a series of selected precursor ions.
| 3. Results | | |
3.1. Determination of total polyphenolic content
Obtained extracts [Table 1] was used to analyze the total polyphenolic content. Total polyphenolic content was calcuted using the content of total hydrolyzable and total condensed polyphenols. Results were shown in [Figure 1]. | Figure 1: Total polyphenolic content obtained by ultrasound extraction of rambutan (mexican variety) husk. Vertical lines of each bar means standard deviation.
Click here to view |
Treatment coded as G1(*), which corresponds to mass/volume ratio 1/7, extraction time 10 min and 10% ethanol/water was the best extraction condition of total polyphenols after ANOVA and Duncan’s test (showed significant statistical differences at P<0.05). Using these conditions, the total polyphenolic content was (487.67±36.01) mg/g [Figure 1] of dry matter. Therefore, this extraction condition was selected to the subsequent experiments.
3.2. ABTS, DPPH and lipid oxidation inhibition assays
The results showed 92.501%, 73.730% and 91.740% of antioxidant activity by ABTS, DPPH, and lipid oxidation inhibition methods of rambutan husk polyphenols obtained with the best extraction condition (G1 treatment) and after Ambertlite XAD-16 chromatography was carried out [Table 2].
3.3. FTIR analysis
A FTIR analysis of the polyphenols obtained with the best extraction condition and after the Amberlite XAD-16 chromatography was carried out to identify the main functional groups of polyphenolic compounds. The signals of the main functional groups of polyphenolic compounds such as hydroxyl groups (3 235.69 cm-1), carboxylic acids (1 702.49 cm-1), aromatic rings (1 445.47 cm-1) and carbonyl group (1 080.80 cm-1) were determined as the most important. The signals are shown in [Figure 2]. | Figure 2: Signals of the main functional groups of polyphenolic compounds from rambutan (mexican variety) husk.
Click here to view |
3.4. Identification of polyphenolic compounds by HPLC/ESI/ MS analysis
Identification profile of polyphenolic compounds of Mexican variety husk was obtained by HPLC/ESI/MS. Compounds identification was carried out using negative ionization as MS operating conditions. Obtained results analysis from Mexican variety husk allowed 12 compounds identification. [Figure 3] showed the chromatogram corresponding to the compounds separated by HPLC, compounds such as corilagin, geraniin and ellagic acid (compounds reported in Mexican variety husk) were identified. [Table 3] showed the compounds identified by ESI/MS. | Figure 3: Chromatographic profile of main compounds in rambutan (mexican variety) husk.
Click here to view |
 | Table 3: Identification of polyphenolic compounds in Mexican variety husk by HPLC/ESI/MS.
Click here to view |
| 4. Discussion | | |
To determinate the total polyphenolic content, we analyzed the contents of hydrolyzable and condensed polyphenols. According to our results, the maximum concentration of phenolic compounds was obtained using a mass/volume ratio 1/7, ultrasound extraction time 10 min and percentage ethanol/water 10% (sample coded as G1). This treatment showed significant differences (P<0.05) after ANOVA and Duncan’s test were done and all experiments were carried out by triplicate. Reports indicated the factor that has a direct influence on polyphenolic compounds extraction is mass/volume ratio[17], because the compounds contained in the evaluated material show greater solute/solvent interaction and extraction rates may increase[18]. Respect to the compounds of Mexican variety husk, it has been reported that using mass/volume ratio of 1/5 around 500 mg/g (dry matter) of total polyphenols are obtained[10].
In the present study, the maximum concentration obtained was 487.67 mg/g. Although the values obtained in this study are lower than previously reported, they are higher compared to other reports with rambutan extracts of Asian origin. Some studies on the ultrasound-assisted extraction of compounds from rambutan not cultivated in Mexico reported total polyphenol content between 200 mg/g and 400 mg/g[19], these quantities are smaller than these quantities reported with Mexican variety husk. However, it has also reported higher amounts of polyphenols in some Asian varieties up to 700 mg/g[20].
The differences found in the polyphenolic contents between Mexican variety and the Asian varieties may be due to cultivation conditions, growth and development of the fruit, for example, climatic and soil conditions[21]. Temperature is a factor that also influences polyphenolic compounds extraction processes[22], generating a greater molecular interaction between the compounds and the extraction solvent. In this study the extraction of the compounds was at room temperature, in spite of this, results obtained here, were similar for the temperature extraction of Mexican variety rambutan compounds previously reported[10]. As mentioned, temperature is important for polyphenols extraction. For this study, the controlled temperature was not used, but ultrasound-assisted extraction technology was used. It has been reported that it is a technology that allows the compounds extraction in adequate yields[19], due to the effects of acoustic cavitation on the sample that cause a better solvent penetration and therefore a greater compounds release from the sample to the solvent[23].
The antioxidant activity of the recovered polyphenolic compounds was evaluated in this study. For the ABTS assay a 92.5% inhibition of this radical was obtained, this means that polyphenolic compounds recovered from Mexican variety rambutan husk showed a high antioxidant capacity. Other studies have reported antioxidant capacities using this radical, however the inhibition values have been lower, these differences are attributed to the evaluated samples origin, especially geographic origin, environmental crop conditions, polpyphenolic compounds concentration and extraction method[20]. Antioxidant activity was evaluated using another radical, DPPH. For this assay a 70.69% inhibition was obtained, this represents a good antioxidant activity using this assay and complements the results obtained with ABTS assay. It has been reported that to determine an adequate antioxidant activity analysis of polyphenolic compounds it is necessary to try both assays[24]. On the other hand, the inhibition of lipid oxidation was evaluated as a complementary analysis for antioxidant activity and an inhibition value of 91.74% was obtained. This test is important for this study because it allows to evaluate the ability of polyphenolic compounds to avoid the oxidation of biomolecules such as lipids, this means evaluated compounds have the potential to prevent human body diseases caused by cellular and molecular oxidation processes[13]. Most of these diseases are degenerative and cause more serious conditions such as the development of different cancer types. In this sense, it has been reported that polyphenolic compounds from rambutan peel are able to inhibit free radicals that related with the development of human mouth-epidermal carcinoma cells and colorectal adenocarcinoma cells (Caco-2)[25].
Once the antioxidant activity of polyphenolic compounds from Mexican variety rambutan husk was determined, compounds identification was carried out using HPLC/ESI/MS. This identification was complemented with FTIR analysis, where the signals of the main functional groups of polyphenolic compounds such as hydroxyl groups (3 235.69 cm-1), carboxylic acids (1 702.49 cm-1), aromatic rings (1 445.47 cm-1) and carbonyl group (1080.8 cm-1) were determined as the most important. Six ellagitannins were identified, of which, 4 have already been reported for Mexican variety rambutan husk[10] and two more were identified in this study. The ellagitannins are recognized for their antioxidant, antimicrobial, anti-cancer properties etc.[14],[26],[27], for that reason they are considered compounds with an important bioactive capacity and are considered as nutraceutical agents. For example, compounds corilagin, geraniin and ellagic acid have been evaluated against pathogenic microorganisms transmitted by food, specifically, against Streptococcus mutans, methicillin-resistant Staphylococcus aureus, Escherichia coli and fungus such as Candida albicans, pathogens that cause diseases in humans[28]. As mentioned above, these compounds also have anticancer capacity against cancer cell lines such as HeLa (cervical cancer)[29], against CLS-354 cells (mouth carcinoma cells)[30]. Their presence in Mexican variety rambutan husk have relevant importance because this material can be used to recover bioactive compounds with medical and pharmaceutical applications. Compounds 1, 4, 5, 6, 8 and 10 are described for first time in Mexican variety rambutan husk. These compounds also have an important bioactive potential; for example, compounds 1 and 4 have been reported as effective agents against the repression of hepatitis C virus, this means that they also possess antiviral activity and represent a potential application for treatment of viral diseases[31]. Compounds 5 and 10 have also been reported as important agents with bioactive potential as antioxidants and antimicrobials[32].
In conclusion, it was demonstrated that the ultrasound-assisted extraction was effective and allowed the recovery of the antioxidant polyphenolic compounds in similar levels to previous reports, it is confirmed that the Mexican rambutan variety husk represents an important source for the recovery of antioxidant polyphenolic compounds. In addition the identification of 12 antioxidant polyphenolic compounds with potential application in the medicine field (as treatment or prevention agents) was achieved.
Conflict of interest statement
We declare that we have no conflict of interest.
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3]
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| Zoé P. Morreeuw,Cristina Escobedo-Fregoso,Leopoldo J. Ríos-González,David Castillo-Quiroz,Ana G. Reyes | | Plant Science. 2021; : 110748 | | [Pubmed] | [DOI] | | | 8 |
High Throughput Profiling of Flavonoid Abundance in Agave lechuguilla Residue-Valorizing under Explored Mexican Plant |
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| Zoé P. Morreeuw,David Castillo-Quiroz,Leopoldo J. Ríos-González,Raúl Martínez-Rincón,Norma Estrada,Elda M. Melchor-Martínez,Hafiz M. N. Iqbal,Roberto Parra-Saldívar,Ana G. Reyes | | Plants. 2021; 10(4): 695 | | [Pubmed] | [DOI] | | | 9 |
Isolation of Polyphenols from Soursop (Annona muricata L.) Leaves Using Green Chemistry Techniques and their Anticancer Effect |
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| Valdez-Guerrero Daisy Yathzamiry,Esparza-González Sandra Cecilia,Morlett-Chávez Jesús Antonio,Nery-Flores Sendar Daniel,Flores-Gallegos Adriana Carolina,Ascacio-Valdés Juan Alberto,Rodríguez-Herrera Raúl | | Brazilian Archives of Biology and Technology. 2021; 64 | | [Pubmed] | [DOI] | | | 10 |
Review of Nephelium lappaceum and Nephelium ramboutan-ake: A High Potential Supplement |
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| Jia Ling Tsong, Lucky Poh Wah Goh, Jualang Azlan Gansau, Siew-Eng How | | Molecules. 2021; 26(22): 7005 | | [Pubmed] | [DOI] | | | 11 |
Early Optimization Stages of Agave lechuguilla Bagasse Processing toward Biorefinement: Drying Procedure and Enzymatic Hydrolysis for Flavonoid Extraction |
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| Zoé P. Morreeuw, Leopoldo J. Ríos-González, Carmen Salinas-Salazar, Elda M. Melchor-Martínez, Juan A. Ascacio-Valdés, Roberto Parra-Saldívar, Hafiz M. N. Iqbal, Ana G. Reyes | | Molecules. 2021; 26(23): 7292 | | [Pubmed] | [DOI] | | | 12 |
Functional and nutritional properties of selected Amazon fruits: A review |
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| Nayara Macêdo Peixoto Araujo,Henrique Silvano Arruda,David Roger Paixão Marques,Williara Queiroz de Oliveira,Gustavo Araujo Pereira,Glaucia Maria Pastore | | Food Research International. 2021; 147: 110520 | | [Pubmed] | [DOI] | | | 13 |
Selection of extraction conditions of phenolic compounds from rambutan (Nephelium lappaceum L.) peel |
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| Nguyen Nhat Minh Phuong,Thien Trung Le,Minh Quan Dang,John Van Camp,Katleen Raes | | Food and Bioproducts Processing. 2020; | | [Pubmed] | [DOI] | | | 14 |
Structural characterization of native and oxidized procyanidins (condensed tannins) from coffee pulp (Coffea arabica) using phloroglucinolysis and thioglycolysis-HPLC-ESI-MS |
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| Jorge E. Wong-Paz,Sylvain Guyot,Pedro Aguilar-Zárate,Diana B. Muñiz-Márquez,Juan C. Contreras-Esquivel,Cristóbal N. Aguilar | | Food Chemistry. 2020; : 127830 | | [Pubmed] | [DOI] | | | 15 |
Solid-State Fermentation with Aspergillus niger GH1 to Enhance Polyphenolic Content and Antioxidative Activity of Castilla Rose (Purshia plicata) |
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| De León-Medina José Carlos,Sepúlveda Leonardo,Morlett-Chávez Jesús,Meléndez-Renteria Paola,Zugasti-Cruz Alejandro,Ascacio-Valdés Juan,Aguilar Cristóbal Noé | | Plants. 2020; 9(11): 1518 | | [Pubmed] | [DOI] | | | 16 |
Preliminary Testing of Ultrasound/Microwave-Assisted Extraction (U/M-AE) for the Isolation of Geraniin from Nephelium lappaceum L. (Mexican Variety) Peel |
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| Cristian Hernández-Hernández,Cristóbal Noé Aguilar,Adriana Carolina Flores-Gallegos,Leonardo Sepúlveda,Raúl Rodríguez-Herrera,Jesús Morlett-Chávez,Mayela Govea-Salas,Juan Ascacio-Valdés | | Processes. 2020; 8(5): 572 | | [Pubmed] | [DOI] | |
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