Assessment of antioxidant activities of HeukHarang a novel Korean Lectuca sativa L.

Abstract

In this study, antioxidant activities of HeukHarang a novel Korean Lectuca sativa L.extracts compair with Red skirt lettuce. The highest total polyphenol contents was 60% ethanol extracts of HeukHarang and total flavonoid contents was 40% ethanol extracts, 84.70 ± 0.11 mg TAE/10 g DW and 63.82 ± 0.09 mg QE/10 g DW, respectively. The highest FRAP activity and PMA were 60% and 80% ethanol extracts of heuharang, 1,876.3 ± 0.01 mM TEAC/10 g DW and 26.2 ± 0.0 mM AAEAC/10 g DW, respectively. Radical scavenging activity also HeukHarang ethanol extracts was higher than Red skirt lettuce. The highest ORAC value was 76.0 ± 0.43 mM TEAC/10 g DWthehd, 100% ethanol extracts of HeukHarang. As a result, the all antioxidant activities of Heuhalang ethanol extracts were higher than that of Red skirt lettuce as a control.

Keywords:
Lectuca sativa L.; Korean lettuce; antioxidant; ORAC assay; FRAP; PMA

1 Introduction

A balanced diet is essential to ensure physical development and health. Numerous epidemiological studies have suggested high daily consumption of fruits and vegetables lowers the risk of several chronic diseases, such as cancer, cardiovascular disease and diabetes; the protective effects of fruit and vegetable consumption are mainly attributed to the presence of bioactive phytochemicals such as polyphenols (Arts & Hollman, 2005; Hooper & Cassidy, 2006; Russo et al., 2012; Chen & Chen, 2013).

Reactive Oxygen Species (ROS), hydroxyl radical, hydrogen peroxide and Superoxide anion etc., leads to DNA denaturation, lipid peroxidation, protein inactivation, and other cell dysfunction. These cause the cancers, diabetes, atherosclerosis and Parkinson's disease (Halliwell et al., 1992). ROS which are directly responsible for oxidative stress, are unstable and highly reactive. Furthermore, these are easily reacted with biomaterials and attacked biomolecules, caused damage to cells and tissues (Lee & Im, 2012). In particular, ROS, was produced by free Radicals (OH^-·, O₂^·), causes aging, inflammation, carcinogenesis, and atherosclerosis (Cho et al., 2008). The human body has biological defense systems such as superoxide dismutase (SOD), glutathione peroxidase (GSH-Px), catalase (CAT), glutathione (GSH) and glutathione S-transferase (GST) to remove these free radicals (Kil et al., 2015). Antioxidants can protect cells from oxidative damage by removing free radicals intermediates and prevent cell apoptosis (Lim, 2010). Synthetic antioxidants such as BHA and BHT have excellent antioxidant effects, however, showed various side effects caused by toxicity; thus, there is increasing interest in research on safe natural antioxidants (Park et al., 2012).

Lettuce (Lactuca sativa L.) is a leafy green vegetable that belongs to Asteraceae family and it is cultivated extensively for food consumption (Abdel Latef et al., 2020). The economically valuable vegetable crop lettuce is a minimally processed food product available throughout the entire year, and is a significant source of natural health promoting compounds (Yang et al., 2017).

Lettuce is of particular interest due to its high antioxidant and phytochemical content (Malejane et al., 2018). Most relevant phytochemicals found in lettuce include vitamin B, vitamin C, vitamin E, carotenoids, and polyphenols. The latter refers to a group of secondary metabolites responsible for the plants’ defense system that has been described to have higher antioxidant capacity than, for example, vitamin C and E (Kim et al., 2016). Although their mechanisms of action are not yet fully understood (Fraga et al., 2019), a large number of epidemiological studies, and their associated meta-analyses, suggested that long-term consumption of diets rich in plant-derived polyphenols and antioxidants offer protection against development of diseases associated to metabolic syndrome, different types of cancer, osteoporosis, and neurodegenerative diseases (Pandey and Rizvi 2009). Chong et al. (2010) reviewed the evidence for the effects of fruit polyphenols on platelet function, blood pressure, vascular function, and blood lipids, all of them risk factors of cardiovascular diseases. The authors of that study concluded that despite the heterogeneity in the design of studies, the lack of controls, and the short intervention periods, there is evidence to suggest that flavonols, anthocyanins, and procyanindins are effective at reducing the above-mentioned risk factors.

In this study, we investigated antioxidant effects of HeukHarang a novel Korean Lectuca sativa L. grown and harvested by the Jeollanamdo Agricultural Research & Extension Services. We extracted HeukHarang by various ethanol concentrations and investigated total polyphenol contents, total flavonoid contents and antioxidative activity evaluation. Furthermore, we intend to provide basic data to ascertain the availability of L. sativa L. as a natural antioxidant material.

2 Materials and methods

2.1 Experimental materials

HeukHarang, a noble lettuce Lactuca sativa L. sample was provided and used from Jeollanamdo Agricultural Research and Extension Services. Folin-Ciocalteu reagent, trolox, gallic acid, catechin, ABTS (2,2'-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid), DPPH (1,1-diphenyl-2-picrylhydrazyl), and L-ascorbic acid were purchased from Sigma-Aldrich Co. (St. Louis, MO, USA). The solvents and all reagents used special-grade reagents.

2.2 Sample extraction

Samples, HeukHarang and red lettuce as a control, pulverized with a grinder (NFM-3561SN, NUC Co., Daegu, Korea) were reflux extracted with distilled water, 20% ethanol, 40% ethanol, 60% ethanol, 80% ethanol, and 100% ethanol for 60 min at 100 °C and filtered. SpeedVac (COSMOS660-50L, Kyungseo Machines Co., Incheon, Korea) was used to concentrate and obtain yields. The concentrated sample was stored at 4 °C before use.

2.3 Total phenolic contents (TPC)

Total polyphenol content (TPC) was measured using the Folin-Ciocalteu colorimetric method (Yun et al., 2018), Hardinasinta et al. (2021) and gallic acid was used as a standard solution. Each extracts (500 µL) was reacted to Folin-Coicalteu reagent (500 µL) for 3 min at room temperature, added to 500 µ of 10% Na₂CO₃ and react for 1 hour, block the light, and then measured at 760 nm with an UV/VIS spectrophotometer (Neogen, Optizen 2120 UV, Sejong, Korea). Total polyphenol contents (mg GAE/g) standard curve was obtained gallic acid (y = 0.0378x + 0.3719, R² = 0.997).

2.4 Total flavonoid contents (TFC)

Total flavonoid contents (TFC) were determined using the Moreno method (Moreno et al., 2000), and catechin was used as a standard solution. Each sample (200 µL) was diluted with 80% ethanol (800 µL). 100 µL of this sample solution was mixed with 5% NaNO₂ (60 µL) for 5 min at room temperature, then added 10% AlCl₃ (60 µL) 5 min at room temperature. After adding 1N NaOH (400 µL), absorbance was measured at 415 nm using a spectrophotometer (Mecasys Co., Daejeon, Korea). Total flavonoid content (mg CE/g) standard curve was obtained catechin (y = 0.0025x + 0.0142, R² = 0.999).

2.5 Ferric-reducing antioxidant power (FRAP)

The ferric-reducing antioxidant power (FRAP) activity was measured by modifying method of Benzie and Strain (1996). The FRAP solution was a mixture of 300 mM acetate buffer (pH 3.6), 10 mM 2,4,6-tripyridyl-s-triazine (TPTZ), and 20 mM FeCl₃·6H₂O. These samples were measured an UV/VIS spectrophotometer (Neogen, Optizen 2120 UV, Sejong, Korea) at 595 nm. The FRAP (mg TE/g) standard curve was obtained Trolox (y=0.0021x-0.0165, R²=0.991).

2.6 Phosphomolybdenum complex assay (PMA)

Spectrophotometric evaluation of antioxidant activity through the formation of a green phosphomolybdenum complex was carried out according to Prieto et al. (1999), El-Sheekh et al. (2021). Sample solutions (100 μL) were combined in an Eppendorf tube with 1 mL of reagent solution (0.6 M sulfuric acid, 28 mM sodium phosphate and 4 mM ammonium molybdate). The tubes were capped and incubated in a water bath at 95 °C for 90 min. After the samples had cooled to room temperature, the absorbance of aqueous solutions of each was measured at 695 nm against a blank. The antioxidant activity (mg AAE/g) standard curve was obtained L-ascorbic acid (y = 0.0021x - 0.0165, R2 = 0.9910) .

2.7 DPPH radical scavenging activity

DPPH radical scavenging activity is one of the methods for measuring the antioxidant activity. It was measured by applying the experimental methods of Yamaguchi et al. (1998). The sample solution (10 μL) and 0.2 mM DPPH (190 μL) were added into a 96-well plate at room temperature for 30 min, and the absorbance was measured at 515 nm using an ELISA reader (Thermo Fisher SCIENTIFIC, Multiskan Sky, Korea). The DPPH radical scavenging activity (mg TE/g) standard curve was obtained Trolox (y = 0.0015x + 2.3996, R² = 0.997).

2.8 ABTS radical scavenging activity

ABTS radical scavenging activity is one of the methods for measuring the antioxidant activity and was measured by applying the experimental method of Thaipong et al. (2006), Liu & Li (2021). A solution of 7.4 mM ABTS and 2.45 mM potassium persulfate was mixed at 37 °C for 24 h. Each sample (150 μL) and ABTS solution (1,350 μL) was reacted in the dark room for 5 min, and measured the UV/VIS spectrophotometer (Neogen, Optizen 2120 UV, Sejong, Korea) at 734 nm. The ABTS radical scavenging activity (mg TE/g) standard curve was obtained Trolox (y = 0.0001x + 0.9179, R² = 0.996).

2.9 ORAC (oxygen radical absorbance capacity) assay

Oxygen radical absorbance capacity value was measured by modifying the experimental method of Talcott & Lee (2002). A sample solution with 75 mM phosphate buffer (pH 7.4) and 100 nM flurescein were treated at 37 °C for 30 min. The reaction was started to add the 34 mM 2,2’-azobis(2-methylpropionamidine) dihydrochloride (AAPH), and fluorescence was measured at 2-minutes intervals for 1 hour under the conditions of excitation 485 nm and emission 535 nm. At this time, the value of the decreasing fluorescence was calculated by the area under the curve (AUC), and the ORAC value was calculated using the decreasing value of the trolox-specific fluorescence.

2.10 Statistical analysis

All experimental results are shown as the mean ± standard deviation (mean ± SD) measured three times. Statistical analysis was performed using the Statistical Package for the Social Sciences (SPSS), and one-way analysis of variance (ANOVA) was performed to test the statistical significance between each experimental group. In cases where differences were observed, Tukey's test was conducted post-test, with p < 0.05 considered statistically significant.

3 Result and discussion

3.1 Total polyphenol and flavonoid contents

Many hydroxyl groups (-OH) in polyphenols are easily bonded to various compounds, so they have excellent antioxidant and anti-cancer effects (Kim et al., 2012). Phenolic compounds contained in fruits provide general quality (such as color and taste) and health functions (such as antioxidant) of plants (Yildiz et al., 2021). They are important ingredients that can protect plants from infections by bacteria and viruses. In this study, total polyphenol contents present in 'HeukHarang' a noble L. sativa ethanol extracts compair with red lettuce as a control were measured using tannic acid as a reference substance (Table 1). Total polyphenol contents ranged from 23.20 to 84.70 mg TAE/10 g DW compair with red lettuce ranged from 23.80 to 75.80 mg TAE/10 g DW. The highest total polyphenol contents among 'HeukHarang' ethanol extracts was 60% ethanol extracts and water, 40%, 60%, 80% ethan0ol extracts were higher than red lettuce as significant (p<0.05) differences.

Table 1
Contents of total polyphenols and flavonoids in water and ethanol extracts of HeukHarang and red lettuce.

Sample		Total polyphenol contents (mg TAE1)/10 g DW2))	Total flavonoid contents (mg QE3)/10 g DW)
HeukHarang4)	water	53.60 ± 0.03b5)6)	50.80 ± 0.09d
	20% EtOH	70.30 ± 0.20c	43.72 ± 0.00c
	40% EtOH	52.00 ± 0.05cd	63.82 ± 0.09f
	60% EtOH	84.70 ± 0.11d	60.30 ± 0.00e
	80% EtOH	73.80 ± 0.17c	61.80 ± 0.00e
	100% EtOH	23.20 ± 0.03a	31.70 ± 0.00b
Red lettuce7)	water	23.80 ± 0.04b	10.25 ± 0.00a
	20% EtOH	75.80 ± 0.06h	34.37 ± 0.00h
	40% EtOH	38.97 ± 0.06e	41.61 ± 0.15i
	60% EtOH	65.58 ± 1.41g	56.69 ± 0.15j
	80% EtOH	48.03 ± 0.06f	33.37 ± 0.09g
	100% EtOH	45.64 ± 0.08f	10.86 ± 0.00a

• ¹⁾
  TAE: tannic acid equivalent;
• ²⁾
  DW: dry weight;
• ³⁾
  QE: quercetin equivalent;
• ⁴⁾
  Newly cultivated lettuce;
• ⁵⁾
  Values are mean ± standard deviation (n=3);
• ⁶⁾
  Values with different letters within the same row are significantly different by Duncan's multiple range test at p<0.05;
• ⁷⁾
  Wild type lettuce.

In the present study, total flavonoid contents of HeukHarang ranged from 31.70 to 63.82 mg QE/10 g DW compair with red lettuce ranged from 10.25 to 56.69 mg TAE/10 g DW. The highest total polyphenol contents among 'HeukHarang' ethanol extracts was 40% ethanol extracts and all extracts were higher than red lettuce as significant (p<0.05) differences.

A noble lettuce, HeukHarang shows the high contents of total polyphenol and flavonoid contents.

3.2 Ferric-reducing antioxidant power (FRAP) and phosphomolybdenum complex assay (PMA)

The FRAP method is a principle in which Fe³⁺ is reduced to Fe²⁺ by directly supplying electrons, and uses a principle in which the ferric tripyridyltriazine [Fe(III)-TPTZ] composite agent is reduced to ferrous tripyridyltriazine [Fe(II)-TPTZ] by an antioxidant (Choi et al., 2005). In this study, the ferric-reducing antioxidant power was measured and converted into TE/10 g DW using Trolox as a standard material and shown in Table 2. Ferric-reducing antioxidant power ranged from 131.1 to 1,876.3 mM TEAC/10 g DW compair with red lettuce ranged from 206.9 to 1,296.2 mM TEAC/10 g DW. The highest ferric-reducing antioxidant power among 'HeukHarang' ethanol extracts was 60% ethanol extracts and all extracts except water extracts were higher than red lettuce as significant (p<0.05) differences.

Table 2
Ferric-reducing antioxidant power and Phosphomolybdenum in water and ethanol extracts of HeukHarang and red lettuce.

Sample		FRAP (mM TEAC1)/10 g DW2))	PMA (mg AAEAC3)/10 g DW)
HeukHarang4)	water	131.1 ± 0.01d5)6)	12.6 ± 0.30e
	20% EtOH	1,337.2 ± 0.01e	11.6 ± 0.30d
	40% EtOH	1,752.2 ± 0.03f	12.9 ± 0.00f
	60% EtOH	1,876.3 ± 0.01g	21.7 ± 0.30g
	80% EtOH	1,340.5 ± 0.02e	26.2 ± 0.00j
	100% EtOH	556.3 ± 0.01b	22.1 ± 0.30h
Red lettuce7)	water	297.5 ± 0.01c	1.1 ± 0.30a
	20% EtOH	1,065.5 ± 0.02i	2.1 ± 0.30f
	40% EtOH	1,121.9 ± 0.02j	1.6 ± 0.00c
	60% EtOH	1,296.2 ± 0.02k	1.3 ± 0.00b
	80% EtOH	934.9 ± 0.01h	3.9 ± 0.79i
	100% EtOH	206.9 ± 0.01a	4.7 ± 1.07k

• ¹⁾
  TEAC: Trolox equivalent antioxidant capacity;
• ²⁾
  DW: dry weight;
• ³⁾
  AAEAC: Ascorbic Acid equivalent antioxidant capacity;
• ⁴⁾
  Newly cultivated lettuce;
• ⁵⁾
  Values are mean ± standard deviation (n=3);
• ⁶⁾
  Values with different letters within the same row are significantly different by Duncan's multiple range test at p<0.05;
• ⁷⁾
  Wild type lettuce.

The PMA method is the principle that Mo(VI) is reduced to Mo(V) by extracts to react with phosphate to form a green phosphate/Mo(V) complex (Prieto et al., 1999). In this study, antioxidant activity was measured using L-ascorbic acid as a standard substance, and it was converted into AAEAC/10 g DW and shown in Table 2. Phosphomolybdenum reduced activity ranged from 11.6 to 26.2 mg AAEAC/10 g DW compair with red lettuce ranged from 1.1 to 4.7 mg AAEAC/10 g DW. The highest phosphomolybdenum reduced activity among 'HeukHarang' ethanol extracts was 80% ethanol extracts and all extracts were higher than red lettuce as significant (p<0.05) differences.

3.3 DPPH and ABTS radical scavenging activity

Antioxidant activity was measured based on DPPH and ABTS free radical scavenging activities widely used to find antioxidants from various natural materials (Lee et al., 2014). DPPH free radical scavenging activity consists in the reduction of DPPH radical by substances present in the extraxts, leading to the formation of reduced DPPH-H, which changes in color from deep purple to loss of color (Chaves et al., 2017). DPPH free radial scavenging activities were measured using DPPH and expressed as trolox equivalent (Guldas et al., 2021). DPPH free radial scavenging activities of HeukHarang extracts used in this experiment were in the range of 727.4 to 804.9 mM TEAC/10 g DW and that of red lettuce were in the range of 299.1 to 341.9 mM TEAC/10 g DW. The highest DPPH free radical scavenging activity among 'HeukHarang' ethanol extracts was 20% ethanol extracts and all extracts were higher than red lettuce as significant (p<0.05) differences.

Another effective method to measure radical scavenging activity is the ABTS radical cation decolorization assay (Dulger Altiner, 2021). This method can be used to obtain results in a short time. It can be applied to both hydrophobic and hydrophilic sample (Kim et al., 2019). ABTS free radial scavenging activities of HeukHarang and red lettuce extracts were compared. Results are shown in Table 3. ABTS free radical scavenging activities of HeukHarang extracts were in the range of 2,305 to 4,405 mM AAEAC/10 g DW, with 60% ethanol extracts showing the highest activity, water, 80%, 100% ethaol extracts were higher than red lettuce. There were significant (p < 0.05) differences in ABTS free radical scavenging activity. These results suggest that antioxidants present in these extracts could eliminate highly reactive free radicals to prevent oxidation of important biomolecules such as unsaturated fatty acids, genes, and proteins (Fan et al., 2011).

Table 3
Antioxidant activities of noble Korean lettuce.

Sample		DPPH (mM TEAC1)/10 g DW2))	ABTS (mM AAEAC3)/10 g DW)
HeukHarang4)	water	781.6 ± 0.05e5)6)	3,305.0 ± 0.00h
	20% EtOH	804.9 ± 0.00b	2,815.0 ± 0.06i
	40% EtOH	792.4 ± 0.00d	3,755.0 ± 0.06g
	60% EtOH	754.1 ± 0.00g	4,405.0 ± 0.06e
	80% EtOH	742.7 ± 0.00i	4,305.0 ± 0.00f
	100% EtOH	727.4 ± 0.00j	2,305.0 ± 0.06j
Red lettuce7)	water	303.0 ± 0.00f	502.0 ± 0.00k
	20% EtOH	318.1 ± 0.00c	6,142.0 ± 0.06c
	40% EtOH	322.3 ± 0.00b	6,482.0 ± 0.00b
	60% EtOH	341.9 ± 0.00a	7,822.0 ± 0.06a
	80% EtOH	322.1 ± 0.00b	3,542.0 ± 0.06d
	100% EtOH	299.1 ± 0.00h	262.0 ± 0.06l

• ¹⁾
  TEAC: Trolox equivalent antioxidant capacity;
• ²⁾
  DW: dry weight;
• ³⁾
  AAEAC: Ascorbic Acid equivalent antioxidant capacity;
• ⁴⁾
  Newly cultivated lettuce;
• ⁵⁾
  Values are mean ± standard deviation (n=3);
• ⁶⁾
  Values with different letters within the same row are significantly different by Duncan's multiple range test at p<0.05;
• ⁷⁾
  Wild type lettuce.

3.4 ORAC assay

The ORAC method, adapted to use fluorescein as fluorescent probe, was used for determine antioxidant activity in vitro in biological samples and foods(Lucas-Abellán et al., 2008). The ORAC assay is the method to determine the radical chain breaking antioxidant capacity by generated AAPH value, thereby showing the advantage of a wide range of applications by reacting both the hydrophobic and hydrophilic components present in samples(Huang et al., 2005; Prior et al., 2003). Relative fluorescence intensity was more active at all extraction concentrations compared to Red skirt lettuce (Figure 1A). ORAC value of HeukHarang extracts used in this experiment were in the range of 66.4 ± 1.3 to 76.0 ± 0.mM TEAC/g DW and that of red skirt lettuce as a control were in the range of 19.9 ± 1.8 to 69.7 ± 3.2 mM TEAC/g DW. The highest ORAC value among 'HeukHarang' ethanol extracts was 100% ethanol extracts and all extracts were higher than red skirt lettuce as significant (p<0.05) differences (Figure 1B).

Figure 1
Relative fluorescence intensity (A) and ORAC value (B) of various ethanol extracts from HeukHarang and Red skirt. (A) Each marks are indicated at various ethanol extract; (B) The values are indicated as means ± standard deviation of three independent experiments. Means with different letters (a-f) are significantly different (p<0.05). 0EE; distilled water extracts, 20EE; 20% ethanol extracts, 40EE; 40% ethanol extracts, 60EE; 60% ethanol extracts, 80EE; 80% ethanol extracts, 100EE; 100% ethanol extracts.

4 Conclusion

To examine the antioxidant characteristics of newly developed Korean lettus, HeukHarang, samples were extracted with different ethanol extraction concentrations. Total antioxidant activity, as Total phenolic contents, total flavonoid contents, Ferric-reducing antioxide power, phosphomolybdenum complex assay, DPPH radical scavenging activity, ABTS radical scavenging activity and ORAC value, of HeukHarang, showed higher than that of Red skirt lettus. The 60% ethanol extract was the most active.

• Practical Application: Research about antioxidant activities and functional products of HeukHarang.
• ^#These authors contributed equally to this work.

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Publication Dates

• Publication in this collection
  01 Apr 2022
• Date of issue
  2022

History

• Received
  03 Jan 2022
• Accepted
  18 Feb 2022