Research Article

Optimization of Ultrasonic Assisted Extraction of Bioactive Compounds from Almond Hull

Nabila Khan1, Imran Ahmad2 and Muhammad Bilal Sadiq1*

1School of Life Sciences, Forman Christian College (A Chartered University), Lahore, 54600, Pakistan; 2Food Agriculture and Biotechnology Innovation Lab (FABIL), Florida International University, Biscayne Bay Campus, North Miami, Florida, USA.

Received | September 12, 2021; Accepted | November 15, 2021; Published | April 28, 2022

*Correspondence | Muhammad Bilal Sadiq, School of Life Sciences, Forman Christian College (A Chartered University), Lahore, 54600, Pakistan; Email: bilalsadiq@fccollege.edu.pk

Citation | Khan, N., I. Ahmad and M.B. Sadiq. 2022. Optimization of ultrasonic assisted extraction of bioactive compounds from almond hull. Sarhad Journal of Agriculture, 38(2): 676-684.

DOI | https://dx.doi.org/10.17582/journal.sja/2022/38.2.676.684

Keywords | Almond hull, Optimization, Antioxidant, Phenolic content, Food by-products

Copyright: 2022 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Almond tree (Prunus amygdalus) is popular nut trees worldwide and belongs to family Rosaceae. In 2019, global almond production was 3.53 million tons and United States of America, Australia, Iran and Italy were recognized as major almond producers (FAO, 2020). Almond hull is the main byproduct of almonds and comprised of 35-62% of fresh almond weight (Prgomet et al., 2017). Almond hulls are assumed as a low economic value byproduct and are mainly used in animal feed. However, almond hulls are rich TPC and can be used for the development of functional food products (Kahlaoui et al., 2019). Almond hull contains antioxidants and exhibits free radical-scavenging potential (Wijeratne et al., 2006). The efficient utilization of agriculture byproducts helps to reduce the environmental hazards associated with organic waste and improved the economic returns (Prgomet et al., 2019a). The food commodities have diverse profile of phenolic compounds and extraction of these polyphenols is dependent on extraction method and extraction parameters. Solvent type, temperature, sample to solvent proportion and time of extraction can greatly influence the phenolic extraction from food matrices (Iglesias-Carres et al., 2018; Zitka et al., 2011). The conventional methods require long extraction time, high temperature and large proportion of solvents, which leads to the degradation of heat sensitive bioactive compounds. Therefore, the concept of modern extraction techniques is gaining interest, such as extraction by ultrasonication and microwave assisted extraction (Guglielmetti et al., 2017). These advance extraction techniques offer less solvent consumption, extraction at low temperature, high yield and purity of target compounds. UAE is inexpensive and simple technique which is achieved at lower temperature and short time by creating acoustic cavitation which disrupts plant cell walls and release of internal cellular constituents into the extraction matrix (Piyalungka et al., 2019). Due to simple, inexpensive and reproducible technique UAE is effective at industrial scale (Sitthiya et al., 2018). The aim of this study was to optimize the UAE of bioactive compounds from almond hull and evaluation of their antioxidant and antimicrobial potential against foodborne pathogens.

Materials and Methods

Sample preparation

Almond fruits were harvested from Hunza valley of Pakistan and hulls were separated manually followed by oven drying for 48 h at 50°C. The samples were ground by mechanical grinder (Philips Co. Ltd., China) and stored at 4°C till further use (Hiranrangsee et al., 2016).

Extraction process

TPC from the almond hull were extracted by UAE and conventional extraction methods.

Conventional extraction

The powdered sample (5 g) was added to ethanol (45 ml; 80%, v/v) and placed in a at 25℃ and 300 rpm in a shaker. The extraction was carried out for 24 and 48 h, separately. The extracts were filtered and stored at 4 °C (Sadiq et al., 2015).

Ultrasonic assisted extraction (UAE)

UAE of almond hull was optimized by RSM using Design-Expert® software (Minneapolis, MN, USA) at a fixed frequency of 20 kHz. UAE was optimized by independent extraction variables, which were sample to solvent ratio (1:20, 1:30 and 1:40 w/v), solvent concentrations (20, 50 and 80%, v/v) and time (10, 20 and 30 min) at fixed temperature of 45°C. TPC and DPPH inhibition were used as response variables (R1 and R2, respectively). The sample was added to beaker containing the extraction solvent and subjected to ultrasonic processor (LSP-500, Industrial Sonomechanics, USA).

TPC and antioxidant activity

TPC was determined using Folin–Ciocalteau regent (Sigma-Aldrich, USA), by following the method described by Sadiq et al. (2015). TPC was estimated by using gallic acid standard curve and presented as mg of gallic acid equivalent (GAE) per gram of raw sample.

Antioxidant potential of almond hull extract was estimated by DPPH inhibition assay by following Sadiq et al. (2015). The extract (50 µl) was added to 5 ml of DPPH in ethanol (40 ppm). The mixture was kept for half an hour in dark at 25℃. After incubation absorbance was measured at 517 nm using UV-Vis spectrophotometer. % DPPH inhibition was calculated using equation 3.

AC: Absorbance of the control (DPPH without extract); AS: Absorbance of sample.

Optimization of UAE extraction

UAE extraction of almond hull was optimized using response surface methodology and optimized run was selected using 0.994 desirability. The optimized extraction conditions were 1:40 g/ml sample to solvent proportion, 22.5 min time of extraction and 80% ethanol (v/v). The optimized extract was lyophilized (Christ Alpha 1-2 LD plus, Germany) to obtain powdered extract.

Characterization of optimized extract

TPC and antioxidant activity: The stock solution (1 mg/ml) of dried extract was diluted with deionized water to 100 μg/ml and TPC was determined using Folin–Ciocalteau regent. Antioxidant potential of optimized extract was determined by DPPH inhibition and FRAP assay. For %DPPH inhibition, different concentrations (31.25-2000 µg/ml) of extract were prepared and %DPPH inhibition was estimated by using equation 3. IC50 values were determined by non-linear regression using GraphPad Prism® version 7. (San Diego, US) (Sadiq et al., 2017). For FRAP assay, almond hull extract (50 μl of 1 mg/ml) was mixed with FRAP reagent (1.5 ml) and incubated at 37°C for 4 min, followed by reading the absorbance at 593 nm. Ferrous sulfate solution (100–1000 μM) was used to develop a standard curve. Ascorbic acid was used as positive control.

Antibacterial activity: Antibacterial activity of almond hull extract was evaluated against Escherichia coli (ATCC 8739), Salmonella typhimurium (ATCC 14028) and Staphylococcus aureus (ATCC 25923). The sterilized cotton swab was used to spread the bacteria (108 CFU/ml) on the surface of nutrient agar plates. The extract (100 µl) in different concentrations (1.56-50 mg/ml) was added into the 8 mm wells made on agar plates. After 24 h incubation at 37 ºC, the inhibition zone diameter was measured. All experiments were performed in triplicates (Taye et al., 2011). MIC of almond hull extract (1.56-50 mg/ml) was estimated by broth macrodilution method following Kubo et al. (2004). After incubation period, the lowest concentration without any visible growth was marked as MIC. MBC was measured by sub-culturing 100 µl of each extract concentrations that had no visible growth on nutrient agar. After 24 h incubation, the minimum concentration without detectable growth on nutrient agar plates was considered as the MBC.

Fourier transform infrared spectroscopy analysis

The optimized extract was characterized by FTIR spectrometer (Agilent technologies, USA). The spectra were recorded (4000-650 cm-1) with a resolution of 4cm-1 using absorbance mode.

GCMS analysis

The optimized extract was analyzed by using GC-MS system (GC-7890A/MS-5975C, Agilent Technologies, Santa Clara, CA, USA) with HP-5 MS capillary column. Helium gas was used as carrier (1.0 ml/min) and sample injection was programmed at 200°C. All data were acquired within the range 50–600 a.m.u. The compounds were identified by using NIST 05 spectral library (Gaithersburg, MD, USA).

Statistical analysis

One-way analysis of variance (ANOVA) and Tukey’s HSD tests were carried out to find significant (p < 0.05) differences among mean observations by using SPSS statistical software package (SPSS, version 23.0).

 

Table 1: Optimization of ultrasound assisted extraction of almond hull and effect of extraction parameters on response variables.

Experiments	Independent variables			Response variables
	Sample to solvent ratio (g/ml)	Time (min)	Ethanol (%)	DPPH inhibition (%)	TPC (mg GAE/g of raw sample)
1	1:20	20	20	68.18 ± 2.1	5.82 ± 0.11
2	1:40	20	20	72.56 ± 2.48	11.13 ± 0.5
3	1:30	20	50	70.07 ± 0.51	8.39 ± 0.2
4	1:40	20	80	86.27±3.41	11.31 ± 0.19
5	1:30	30	80	82.10 ± 1.66	7.94 ± 0.12
6	1:30	30	20	73.27 ± 1.48	7.10 ± 0.35
7	1:20	20	80	81.26 ± 2.31	4.92 ± 0.5
8	1:30	10	80	73.20 ± 0.92	8.02 ± 0.193
9	1:40	30	50	83.66 ± 2.77	9.75 ± 0.4
10	1:30	20	50	76.01 ± 1.68	7.50 ± 0.36
11	1:30	20	50	76.15 ± 0.51	7.44 ± 0.31
12	1:40	10	50	75.72 ± 0.51	9.76 ± 0.32
13	1:20	30	50	77.65 ± 0.35	5.31 ± 0.12
14	1:30	10	20	67.66 ± 3.31	7.29 ± 0.4
15	1:20	10	50	68.91 ± 0.76	5.09 ± 0.11

 

Results and Discussions

UAE and conventional extraction of almond hull

UAE and conventional solvent extractions were used for the extraction of TPC. The conventional extraction resulted in TPC and %DPPH inhibition of 2.67 ± 0.17 mg GAE/g of raw almond hull and 63.89 ± 0.45%, respectively after 24 h of extraction, whereas, after 48 h of extraction the TPC and %DPPH inhibition were 2.56 ± 0.27 mg GAE/g and 64.34 ± 1.97%, respectively. UAE extraction of almond hull was optimized by using Box-Behnken design (Table 1). The optimal extraction conditions were 1:40 sample to solvent ratio, 80% ethanol and 20 min of extraction time which corresponded to TPC and %DPPH inhibition of 11.31 ± 0.19 mg GAE/g and 86.03 ± 3.41%, respectively. As compared to conventional solvent extraction, UAE was found to be more effective and rapid for TPC extraction. The reported difference in yield of TPC by conventional and UAE extractions might also be influenced by different extraction conditions such as extraction time, sample to solvent ratio and extraction temperature. UAE is based on the application of sound waves to disrupt plant membranes, which facilitates the solvent penetration and enhance the high extraction yield (Mala et al., 2021). Similarly, He et al. (2016) found high yield of TPC and antioxidant activity in blueberry wine pomace after UAE in comparison to conventional extraction.

Effect of UAE extraction parameters on TPC

TPC of almond hull extract was in the range of 4.92 ± 0.5 to 11.31 ± 0.19 mg GAE/g of raw material. Quadratic model was used to evaluate the effect of extraction parameters on response variables. The sample to solvent proportion significantly effect (p < 0.05) TPC in comparison to solvent concentration and UAE extraction time. The polynomial equation for TPC is presented as equation 1.

X1: Sample to solvent ratio; X2: Extraction time; X3: Solvent concentration.

The p-value of 0.0042 and R2 (coefficient of determination) value of 0.9641 indicated that the model was significant. Ingawale et al. (2018) reported that the hydroalcoholic solvent was more effective for the extraction of TPC than alcohol alone and increase in concentration of alcohol resulted in an increase in TPC. Simsek et al. (2012) reported that TPC was increased with an increase in extraction time of sour cherry pomace to optimal time and further increase in time, decreased the TPC. Extended extraction time might enhance the exposure of phenolics to oxygen and light, which resulted in degradation of the antioxidants. The extraction of TPC from Murtus communis L. leaves and milled berries was reported to increase with an increase in sample to solvent ratio (Cacace et al., 2003; Dahmoune et al., 2015). The increase in sample to solvent proportion results in an increase mass transfer, hence extraction yield is improved (Pinelo et al., 2007).

Effect of UAE extraction parameters on %DPPH inhibition

Antioxidant activity of almond hull extract was in the range of 67.54 ± 0.51 to 86.03±3.41%. Quadratic model was used to evaluate the effect of extraction parameters on %DPPH inhibition. All the extraction parameters (sample to solvent proportion, extraction time and solvent concentration) had significant effect (p < 0.05) on %DPPH inhibition. The sample to solvent proportion, extraction time and concentration of solvent were reported to significantly influence the antioxidant activity (Belwal et al., 2016; Chavan and Singhal, 2013). The polynomial equation for %DPPH inhibition is presented as equation 2.

X1: Sample to solvent ratio; X2: Extraction time; X3: Solvent concentration.

The p-value (0.0420) and R2 (coefficient of determination) value of 0.9035 indicated that the model was significant.

Optimization of UAE extraction

UAE extraction conditions were optimized by using optimization function of Design expert and optimized extraction conditions (1:40 g/ml, sample to solvent ratio, 22.5 min extraction time and 80% ethanol) with desirability of 0.994 were used for TPC extraction. The optimized extract was evaluated for its bioactive potential.

Characterization of optimized extract

TPC and DPPH inhibition: TPC of optimized extract was 110.17 ± 3.44 mg of GAE/g of dried extract. Sfahlan et al. (2009) reported TPC of almond hull extract as 78.2 mg GAE/g, which was lower than the current investigation. Prgomet et al. (2019a) reported TPC of almond hull extract in the range of 91.76-138.9 mg GAE/g of extract. The reported variations in TPC depends on plant species, environmental conditions, postharvest processing, maturity of fruit and collection season (Sadiq et al., 2015). The antioxidant activity increased with concentration and the highest DPPH inhibition (87.45 ± 1.28%) was observed at 2000 µg/ml, whereas, the lowest DPPH inhibition (44.17 ± 1.91%) was observed at 31.25 µg/ml (Figure 1). Positive control (vitamin C) exhibited 95.03 ± 0.81% DPPH inhibition at 2000 µg/ml. The corresponding IC50 values for almond hull and vitamin C were 51. 64 and 180 μg/ml, respectively. Qureshi et al. (2019) reported IC50 value of almond hull extract as 167.11 and 76.04 μg/ml for 70% ethanol extract and n-butanol fraction, respectively. FRAP values of optimized almond hull extract and vitamin C were 3625.5 ± 66 and 3530 ± 96 μM of Fe (II)/g, respectively. Tlili et al. (2019) reported that almond hulls contain bio-antioxidants which can be used in food and feed industries.

 

Antimicrobial activity: The antimicrobial activity of almond hull extract was increased with the increase in extract concentration (Table 2). The maximum diameter of inhibition zones was 19.66 ± 0.58, 19.67 ± 0.58 and 19.33 ± 1.15 mm against E. coli, S. typhimurium and S. aureus, respectively, at the highest test concentration (50 mg/ml). MIC value of almond hull extract was 12.5 mg/ml against all test bacteria. MBC value of almond hull extract was 12.5 mg/ml for E. coli and S. aureus, whereas it was 25 mg/ml for S. typhimurium. Polyphenolic compounds present in almond hull were reported to exhibit antimicrobial potential (Prgomet et al., 2019b). Antibacterial mechanism of polyphenolic compounds is associated with their ability to form hydrogen bonding with cell membrane proteins, destruction of electron transport chain and disruption of membranes (Liaqat et al., 2019).

 

Table 2: Antimicrobial activity of almond hull extract.

Concentration	Diameter of zone of inhibition against pathogens
mg/ml	Escherichia coli (mm)	Salmonella typhimurium (mm)	Staphylococcus aureus (mm)
50	19.66 ± 0.58a	19.67 ± 0.58a	19.33 ± 1.15a
25	18.33 ± 1.53a	15.33 ± 1.53b	16.33 ± 1.53a
12.5	12.66 ± 1.15b	13.67 ± 1.53bc	15.33 ± 1.53ab
6.25	10.66 ± 1.53b	11.33 ± 2.08c	11 ± 2.65b
3.12	-	-	-
1.56	-	-	-

Where, - indicate that there was no inhibition. Different superscript letters (a-c) indicate significant differences (p < 0.05) among mean observations within columns.

 

FTIR analysis of almond hull extract

FTIR spectrum of extract was summarized in Table 3 and Figure 2. The peaks in the range of 2936-2913 cm-1, 1618-1498 cm-1, 1377-1233 cm-1, 900-700 cm-1 and 1040-1030 cm-1 were attributed to aliphatic compounds, aromatic compounds, carboxylic acid, aromatic hydrocarbons and aliphatic ethers, respectively (Geetha et al., 2019). The presence of several hydroxyl groups on aromatic ring provides ability to polyphenolic compounds to donate a proton to a radical and act as an antioxidant or chain breaking molecule upon secondary oxidation (Franco et al., 2008).

GCMS analysis of almond hull extract

The major phytoconstituents identified in almond hull extract were β-sitosterol (44 %), diisooctyl phthalate (12%), benzene, 1,3-bis (1,1-dimethylethly) (9.9%), phenol, 2,4-bis (1,1-dimethylethly) (8.7%), n-hexadecanoic acid (8%), 9-octadecenamide, (Z) (7%), spirost (5.20%) and lupeol (4.9%). β-sitosterol and its glucoside derivatives were reported for lowering cholesterol, cancer prevention, antimutagenic and anti-inflammatory effects (Villasenor et al., 2002). Lupeol and hexadecanoic acid were previously reported as strong antioxidants (Jiang et al., 2017; Srivastava et al., 2013).

 

Table 3: Assignment of FTIR peaks to the functional groups present in almond hull extract.

Range (cm-1)	Group and class of compound	Assignment and remarks	Almond hull extract (cm-¹)
2936-2913	CH3—CH2 In Aliphatic compounds	CH3—CH2— Anti-symmetric stretch	2929.7
1697	C=O	—C=O stretch	1688.5
1600-1520	NH3+ In NH4OH	NH3 Deformation	1580.4, 1524.5
1618-1498	Benzene ring in aromatic compounds	C=C Aromatic ring stretch	1580.4, 1524.5
1550-1475	N—O Nitro compounds	N—O Asymmetric stretch	1524.5
1427	O—H In carboxylic acid	O—H stretch	1440.6
1233-1377	C—O In carboxylic acid	C—O stretch	1390.3, 1284.1
1246.92	O—H In carboxylic acid	O—H stretch	1248.7
1040-1030	C—O—C In aliphatic ethers, Si—O In silicates	C—O—C Asymmetric stretch, Si—O stretch	1041.8
900-700	=CH In aromatic hydrocarbons	=C—H out of plane bending	877.79, 820.01, 765.97

 

Parvez et al. (2018) reported that phytoconstituents such as β-sitosterol and lupeol exhibit antimicrobial and antioxidant potential.

Conclusions and Recommendations

This study was aimed to optimize the conditions that provide the maximum yield of TPC and high DPPH inhibition of almond hull extract. The optimized ultrasonic assisted extraction conditions for almond hull extract were with 80% ethanol for 20 min and 1:40 solid to solvent ratio to achieve the maximum output response. Almond hulls were found good source of phenolics, exhibited high DPPH inhibition and showed considerable inhibition of food borne pathogens. Due to antioxidative and antimicrobial potential, almond hull extract can be used as a natural source of preservative for food and feed applications.

Acknowledgements

The manuscript has not been submitted or published anywhere. All authors agree contribute significantly and agree to submit manuscript to Sarhad Journal of Agriculture.

Novelty Statement

The research study highlights the importance of almond hull which is byproduct of almond processing, as a potential functional ingredient in food and feed.

Authors’ Contributions

Nabila Khan: Performed all the experiments.

Muhammad Bilal Sadiq: Supervised the research and designed the experimental plan.

Imran Ahmad: Performed data analysis and manuscript drafting.

Conflicts of interest

The authors have declared no conflict of interest.

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