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. 2022 Oct 2;32(2):221–228. doi: 10.1007/s10068-022-01175-z

Screening of antioxidant capacity of Nepali medicinal plants with a novel singlet oxygen scavenging assay

Chan Seo 1, Hyun Woo An 2, Won Han 3, Joo Won Lee 2, Krishna K Shrestha 4, Won-Kyo Jung 5,6, Joong Ho Shin 3,5, Sang Gil Lee 1,2,✉
PMCID: PMC9839913  PMID: 36647521

Abstract

Pollutant exposure due to industrial development increases oxidative stress in human bodies. Dietary intake of antioxidant shows a protective effect against oxidative damage induced by oxidative stress. Therefore, the development of natural antioxidants is needed. In this study, the antioxidant activities of some Nepali medicinal plant extracts were measured. Using Rose bengal and 3,3′,5,5′-tetramethylbenzidine, a novel assay was utilized to evaluate the singlet oxygen scavenging capacity, and showed a strong correlation with other antioxidant assays. Also, antioxidant capacities based on four assays including the singlet oxygen scavenging assay were highly correlated (≥ 0.858) with the total phenolic contents in the medicinal plant extracts. Among the selected extracts, Persicaria capitata, Elaphoglossum marginatum and Eurya acuminata showed the highest antioxidant capacities. Overall, this study presents a novel approach for evaluating singlet oxygen scavenging capacity, and performed a screening of antioxidant capacities of 54 Nepali herbal medicines.

Supplementary Information

The online version contains supplementary material available at 10.1007/s10068-022-01175-z.

Keywords: Singlet oxygen scavenging capacity, Medicinal plant, Antioxidant, Total phenolic content, Rose bengal

Introduction

Mitochondrial energy metabolism and innate immune system produce various reactive oxygen species (ROS), such as superoxide radicals, hydroxyl radical and singlet oxygen (1O2) (Ott et al., 2007). Exposure to pollutants including heavy metals and pesticides also causes the production of ROS (Limón-Pacheco and Gonsebatt, 2009). Human bodies have a mechanism to keep the ROS homeostasis. However, if the antioxidant system loses its homeostatic capacity, oxidative stress caused by ROS can be detrimental (Ott et al., 2007). Several studies have reported that oxidative stress contributed to the incidence of many chronic diseases, such as cancer, Alzheimer's disease, and diabetes (Bonda et al., 2010; Sosa et al., 2013; Yang et al., 2011). In addition, decreased activity of antioxidant-related enzymes and increased oxidative level during aging have been observed (Junqueira et al., 2004).

Among various types of ROS, 1O2 is produced by photosensitization reaction and normal metabolic process in the body (Onyango, 2016; Winterbourn and Kettle, 2013). 1O2 has non-radical and electrophilic properties and induces oxidation reactions with organic compounds (Agnez-Lima et al., 2012). 1O2 maintains cellular metabolism through regulating cell signaling, including JNK and NF-κB pathways (Clo et al., 2007; Legrand-Poels et al., 1995). However, over accumulated reactive 1O2 can damage nucleic acids or distort cellular calcium homeostasis (Agnez-Lima et al., 2012; Cadet et al., 2008; Krieger-Liszkay et al., 2008). Especially, guanine of nucleic acid is easily oxidized by 1O2 which can lead to DNA mutation (de Biologia et al., 1992; Menck et al., 1993). In addition, 1O2 induces mitochondrial depolarization and lysosomal destabilization in organelles (Ray et al., 2013). Polyphenols, carotenoid and tocopherols, well-known secondary metabolites of plants, have strong redox capacity to scavenge free radicals and 1O2 (Bors and Michel, 2002; Devasagayam and Kamat, 2002). Thus, plants have a potential to be utilized as natural medicines for treating oxidative stress related diseases (Shim et al., 2005). However, the evaluation of singlet oxygen scavenging capacity of plants is very insufficient because there is absence to method of measuring single oxygen generation and erasure.

Nepal has been known as a country with many valuable medicinal plants growing in Nepal Himalayas. Table 1 shows a list of Nepali medicinal plants which are traditionally used for therapeutic purposes, such as to treat stomach disorder, antipyretics, wound healing, and skin diseases. However, comprehensive comparisons of their antioxidant capacities are very limited. Especially, examination of 1O2 scavenging capacities of Nepali medicinal plants were limited.

Table 1.

List of medicinal plant from Nepal

No Registrationa Family Genus Curative uses
1 FBM174-049 Acanthaceae Barleria Swelling
2 FBM174-050 Amaranthaceae Amaranthus Diarrhea
3 FBM179-078 Apocynaceae Cryptolepis Blood purifier, scabies
4 FBM174-035 Asteraceae Dichrocephala Cuts and wound, malarial fever, sinusitis, migrane
5 FBM174-038 Crassocephalum Diarrhea, cuts and wound
6 FBM174-041 Ageratum Cuts and wounds
7 FBM179-065 Tridax Insomnia
8 FBM191-005 Elephantopus Jaundice
9 FBM191-018 Eclipta While discharge in urine, scabies
10 FBM191-019 Taraxacum Asthma, fever
11 FBM191-024 Galinsoga Cuts
12 FBM198-006 Xanthium Tonic, Diuretic
13 FBM198-007 Tagetes Boils
14 FBM198-015 Anaphalis Cut and wounds
15 FBM198-016 Sonchus To check bleeding from mouth and nose
16 FBM174-051 Boraginaceae Cynoglossum Cuts and wounds
17 FBM191-009 Caprifoliaceae Dipsacus Cough
18 FBM174-054 Dryopteridaceae Elaphoglossum Stomach disorder
19 FBM179-066 Equisetaceae Equisetum Burning micturition, cooling agent
20 FBM198-008 Sprain, bone dislocation
21 FBM174-045 Euphorbiaceae Euphorbia Boils
22 FBM191-091 Fabaceae Uraria Diarrhea
23 FBM174-052 Gentianaceae Swertia Fever
24 FBM174-060 Lamiaceae Scutellaria Stomatitis (boils in tongue), fever
25 FBM179-053 Pogostemon Cough and running nose
26 FBM191-010 Leucas Stomach pain
27 FBM191-012 Mentha Boils
28 FBM191-023 Rabdosia Cuts and wounds
29 FBM191-084 Rabdosia Cuts
30 FBM198-014 Mentha Boils, cuts and wound
31 FBM191-096 Linaceae Reinwardtia Headache
32 FBM191-095 Lythraceae Cuphea Cuts
33 FBM191-007 Piperaceae Piper Cough, Chest problem
34 FBM198-017 Throat pain
35 FBM174-042 Plantaginaceae Plantago Indigestion
36 FBM174-040 Polygonaceae Persicaria Stomach pain
37 FBM174-065 Boils, wound
38 FBM191-086 Backache
39 FBM191-087 Skin diseases
40 FBM174-070 Polypodiaceae Drynaria Backache, bone dislocation
41 FBM191-092 Ranunculaceae Clematis Toothache, cuts and wounds
42 FBM191-097 Stomach pain
43 FBM174-075 Rubiaceae Rubia Skin disorder, boils, joint pain
44 FBM179-069 Toothache
45 FBM198-009 Rutaceae Zanthoxylum Stomach pain, constipation, anthelmintic
46 FBM179-063 Solanaceae Solanum Vomiting, stomach disorder and child sickness
47 FBM191-099 Physalis Diuretic
48 FBM191-008 Pentaphylacaceae Eurya Skin diseases
49 FBM174-081 Urticaceae Boehmeria Cuts and wound
50 FBM191-089 Caprifoliaceae Valeriana Rheumatism
51 FBM191-076 Lamiaceae (Verbenaceae) Lippia Fever
52 FBM191-079 Vitex Stomach disorder, Rheumatism
53 FBM191-085 (Verbenaceae) Lantana Rheumatism
54 FBM174-076 Vitaceae Tetrastigma Bone dislocation
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aRegistered number for identification of extract samples in IBMRC

Generally, 1,3-diphenylisobenzofuran (DPBF) is used as a probe for measuring 1O2 scavenging capacity (Żamojć et al., 2017). However, since DPBF has high reactivity with 1O2, it can be oxidized in the presence of an antioxidant such as vitamin C. Also, it easily reacts with other ROS such as H2O2, thus DPBF lacks specificity for 1O2. Kim et al. (2013) reported that singlet oxygen sensor used in fluorescence spectroscopy generates singlet oxygen by visible-light (532 nm). Thus, an error may occur in result of 1O2 scavenging capacity. In addition, N,N-dimethyl-4-nitrosoaniline, NaOCl and H2O2 can be used to measure the amount of 1O2 (Mandal et al., 2011). N,N-Dimethyl-4-nitrosoaniline is bleached by 1O2, and has an absorbance of 440 nm. However, H2O2 is sensitive to temperature and pH, so it is easy to decompose, and the stability to the generation of 1O2 may decrease (Wilson et al., 2017). Thus, it would be useful to use directly singlet oxygen source for measuring scavenging capacities of antioxidant compounds. Rose bengal (RB), an organic stain, is a widely used highly efficient 1O2 producer (Estevão et al., 2015; Facchin et al., 1991; Lin et al., 2013). By exciting RB with 525 nm light, 1O2 can be generated. Also, 1O2 can oxidize 3,3′,5,5′-tetramethylbenzidine (TMB), a chromogenic substrate, directly or through accelerating the generation of hydroxyl radical from hydrogen peroxide. Therefore, our study aimed to measure 1O2 scavenging capacities of fifty-four Nepali medicinal plant extracts using a novel and convenient analysis method with RB and TMB, and to examine its correlation with other antioxidant capacity measurement assays.

Materials and methods

Chemicals and reagents

Gallic acid, ascorbic acid (vitamin C), Folin-Ciocalteu’s (FC) reagent, 2,2′-azobis(2-amidinopropane) dihydrochloride (AAPH), 2,4,6-tri[2-pyridyl]-s-triazine (TPTZ) phosphate-buffered solution (PBS), citric acid, sodium acetate and 2,2-diphenyl-1-picrylhydrazyl (DPPH) were purchased from Sigma-Aldrich (Saint Louis, MO, USA). Sodium carbonate (Na2CO3) was purchased from Tokyo Chemical Industry (Tokyo, Japan). 2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS) was purchased from ROCHE (Mannheim, Germany). RB and TMB were purchased from Alfa Aesar (Karlsruhe, Germany) and Thermo Fisher Scientific (Waltham, MA, USA).

Sample preparation

Total 54 standardized whole plant extract powders were obtained from International Biological Material Research Center (IBMRC) in the Korea Research Institute of Bioscience and Biotechnology (KRIBB). The plant extract stock solutions were diluted to 30 mg/mL with methanol. For analysis, working solutions were prepared at three concentrations as indicated. The academic name of plants was indicated as Registration ID, Family, and Genus for a natural resource security except for three samples with significantly high anti-oxidative capacity.

Rose bengal assay for singlet oxygen scavenging capacity

In order to analyze all the samples in the same batch, a 96-well-based LED radiation system based on Arduino was devised (Fig. 1). RB was selected the maximum concentration that linearly increased 1O2 at 100 µg/mL of TMB. Briefly, 60 µL of deionized distilled water and 130 µL of TMB solution (100 µg/mL) were added to a 96-well black clear-bottom plate. Subsequently, 20 µL of each extract or different concentrations of vitamin C as a standard compound and RB reagent (100 µg/mL) were added and mixed at 500 rpm for 1 min on a microplate shaker. And then, light for singlet oxygen generation was irradiated at 530 nm for 30 min, and absorbance was measured at 650 nm every 5 min. The area under curve (AUC) of absorbance values were calculated and the singlet oxygen scavenging capacities were expressed as mg vitamin C equivalent (VCE)/g dry weight.

Fig. 1.

Fig. 1

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(A) Circuit diagram of the device using Arduino. (B) LED plate made with Arduino base. (C) 530 nm LED irradiation

Total phenolic content

Total phenolic content (TPC) in 54 plant extracts was measured by colorimetric assay with Folin-Ciocalteu (F–C) reagent (Baek et al., 2021). Briefly, an aliquot of 10 µL of extracts were mixed with 130 µL of deionization distilled water and 10 µL of F–C reagent in a 96-well plate, and reacted for six min. After reaction, 100 µL of 7% Na2CO3 solution was added. The absorbance of the mixture at 750 nm was measured using microplate reader (Multiskan, Thermo Scientific, USA) after 90 min incubation at room temperature. TPC in plant extracts were expressed as mg gallic acid equivalents (GAE)/g dry weight.

DPPH radical scavenging assay

The DPPH radical scavenging assay was performed according to a modified Blois, M. S. method (Brand-Williams et al., 1995). For the DPPH assay, 2,2-diphenyl-1-picrylhtdrazyl (DPPH) was made at 0.1 mM in 80% (v/v) aqueous methanol. Subsequently, the absorbance of DPPH radical solution was adjusted as 0.700 ± 0.020 with 80% methanol at 517 nm. Five microliters of diluted 54 samples were added to 96-well plate with 245 µL of DPPH solution. Mixtures were shaken and incubate for 30 min in the dark at room temperature. After incubation, the absorbance at 517 nm for DPPH was measured. The DPPH radical scavenging capacity of plant extracts was expressed as mg VCE/g dry weight.

ABTS radical scavenging assay

ABTS radical scavenging assay was performed slightly modified method from the van den Berg method (Van den Berg et al., 1999). Subsequently, 10 and 2.5 mM of AAPH and ABTS was mixed with 100 mL of phosphate buffer solution. The mixture was heated in a water bath at 80 °C for 40 min to generate ABTS radical. The radical solution was diluted with phosphate buffer solution to make the absorbance at 734 nm between 0.700 ± 0.020 after filtered using 0.45 μm PVDF filter. Diluted 56 sample extracts of 10 µL was mixed with 240 µL of ABTS radical solution on 96 well plate. The mixture was incubated at 37 °C for 10 min. The decrease in absorbance at 734 nm was measured after incubation. The antioxidant capacity of plant extracts from Nepal was expressed as mg VCE/g dry weight.

Ferric reducing antioxidant power (FRAP)

The FRAP assay for medicinal plant of Nepal was carried out according to the procedure of Benzie and Strain with slight modification (Benzie and Strain, 1996). The FRAP reagent was prepared by mixing 200 mL of acetate buffer (300 mM, pH 3.6) with 20 mL of 10 mM TPTZ, 20 mL of 2 mM FeCl3 and 24 mL of distilled water. FRAP reagent was prepared fresh daily and was kept at 37℃ in a water bath until use. Diluted samples of 6 μL was added to 96-well plate with 200 μL of the FRAP reagent. The absorbance was measured at 593 nm. Ferrous sulphate (FeSO4) was used to make a standard curve (0.1 mM to 1.0 mM). The reducing power was expressed as mM FeSO4 equivalent/g dry weight.

Statistical analysis of data

Data were presented as mean ± SD of at least triplicated experiments. Heatmap analysis was conducted to express the antioxidant capacities and total phenolic contents of the 54 samples using the R statistical system (http://www.R-project.org/, version 4.1.0). Pearson’s correlation coefficient was calculated using GraphPad Prism (GraphPad Software, San Diego, CA, USA, version 9.0.0).

Results and discussion

Total phenolic contents

Various phenolic compounds of plants exert many physiological activities such as anti-inflammatory, antibacterial, and antioxidant (Caleja et al., 2017; Durazzo et al., 2019). The antioxidant effect is attributed to the hydroxyl groups in the structure of phenolic compounds, and the content of the phenolic compound in samples is positively correlated with its antioxidant activity (Caleja et al., 2017). In this study, TPC of 54 medicinal plants from Nepal was measured by Folin-Ciocalteu’s method (Baek et al., 2021), and the results showed in Fig. 2 as a heatmap analysis and Supplementary Table 1. The TPC of 54 extracts ranged from 8.9 (sample No.29) to 328.1 (sample No.37) mg GAE/g dry weight. Among them, TPC was highest in Persicaria capitata (Buch-Ham. ex D. Don) H. Gross (No. 37, 328.1 ± 7.0), followed by Elaphoglossum marginatum (Wall. ex Fee) T. Moore (No. 18, 306.8 ± 5.0) and Eurya acuminata DC. (No. 48, 221.0 ± 2.8). The TPC of the plant depends on the extraction method, the extraction site, and the collection area (Benabderrahim et al., 2019; Romani et al., 2003). Our results showed, in a good agreement with other studies, that P. capitata (No. 37) and E. acuminata (No. 48) had significantly higher TPC levels than other Nepali plants. According to one study, P. capitata (No. 37) had the highest flavonoid content (74.6 mmol trolox/100 g dry weigh) among 3 types Persicaria genus in Nepal (Huang et al., 2008). In addition, Seal (2014) compared the TPC levels of seven leaf extracts including E. acuminata (No. 48) and reported that E. acuminata (No. 48) had the highest TPC level than the other leaf extracts with a 487 mg GAE/g dry weight.

Fig. 2.

Fig. 2

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Heatmap analysis of antioxidant capacity for medicinal plant from Nepal

Comparison of antioxidant capacities of Nepali plant extracts

1O2 scavenging capacities of 54 extracts was measured using spectrophotometry assay with RB and TMB (Fig. 2 and Supplementary Table 1). The structure of TMB is consisted of a benzidine with two amine groups. These amine groups of TMB can be oxidized by ROS including 1O2 and hydroxyl radical which results in color change yellow to blue (Cao et al., 2021; Olgun et al., 2018; Zhang et al., 2020). H2O2 has been used as a redox mediators for TMB in many studies for generating hydroxyl radicals (Chen et al., 2019; Wang et al., 2017). Serving as a photosensitizer, RB has high efficiency to generate 1O2 (Estevão et al., 2015). When RB is irradiated with green light of LED at 530 nm, it becomes excited and reacts with oxygen in the atmosphere to produce 1O2 (Brame et al., 2014; Estevão et al., 2015; Zhang et al., 2015). 1O2 generated by RB can directly oxidize TMB. Thus, this method is to measure antioxidants capable of scavenging 1O2, and proposed as a method for measuring oxidized TMB by 1O2. AUC for 30 min LED irradiation showed various range from 69.4 to 2166, and top three species with the highest AUC were P. capitata (No. 37, 2166.7 ± 28.7), Euphorbia hirta (No. 21, 1483.3 ± 31.6) and E. marginatum (No. 18, 1415.4 ± 29.2).

The DPPH, ABTS, and FRAP assays are the most commonly used methods to measure total antioxidant capacities. The DPPH and ABTS assay are used to measure radical scavenging capacities of tested samples through decolorization of radical compounds (Alam et al., 2013; Boligon et al., 2014; Brand-Williams et al., 1995), while FRAP assay examines their reducing powers (Cerretani and Bendini, 2010; Prior et al., 2005). Total antioxidant capacities of 54 Nepali medicinal plant extracts by those three assays were expressed as heatmap analysis for visual explanation (Fig. 2) as well as Supplementary Table 1. For the DPPH radical scavenging activity, P. capitata (No. 37) showed the highest total antioxidant capacity among the 54 samples as 165.9 ± 14.3 mg VCE/g dry weight, followed by E. acuminata (No. 48, 126.1 ± 2.2), and Euphorbia hirta (No. 21, 98.6 ± 0.5). P. capitata (No. 37) and E. acuminata (No. 48) also showed the highest and the second highest ABTS radical scavenging capacities as 664.0 ± 32.7 and 419.3 ± 13.8 mg VCE/g dry weight, respectively. And, E. marginatum (No. 18, 402.2 ± 24.9) showed the third highest ABTS radical scavenging capacity. In the case of FRAP assay, P. capitata (No. 37, 8204.8 ± 286.2 mM FeSO4 equivalent/g dry weight) exhibited the highest reducing power followed by E. marginatum (No. 18, 4040.1 ± 455.3) and E. acuminata (No. 48, 3942.5 ± 282.2).

The heatmap analysis clearly showed the difference in antioxidant oxidative capacity of 54 extracts, in particular, P. capitata (No. 37) showed the distinctly highest antioxidant activity among the 54 samples. Among the rest, E. marginatum (No. 18) and E. acuminata (No. 48) showed significantly outstanding antioxidant capacities. As herbal medicines, P. capitata, E. marginarum, and E. acuminata are used for treating boils, stomach disorder, and skin diseases, respectively. Oxidative stress has been implicated in the progress of all those diseases (Forman and Zhang, 2021). The strong antioxidant capacity of the plants might contribute to their therapeutic effects on those conditions.

A Pearson correlation analysis was performed to determine the association between the RB assay and the other antioxidant assays (Table 2). RB assay showed significantly positive correlation with DPPH, ABTS, and FRAP assays which indicates that compounds having strong total antioxidant capacities also show strong singlet oxygen scavenging capacities. This suggested that the major antioxidant components in the samples are polyphenols. In practice, the correlations between TPC and readings from four antioxidant capacity assays including RB, DPPH, ABTS and FRAP were high as r = 0.858, 0.893, 0.928 and 0.908, respectively. This finding indicates that polyphenols are major antioxidants in the Nepali medicinal plant extracts (Sachindra et al., 2010; Xu et al., 2007). Our study also confirmed that RB assay could be a simple and reliable method for measuring 1O2 scavenging capacity.

Table 2.

Correlation between TPC and four antioxidant capacity values

TPC DPPH ABTS FRAP RB
TPC 1 0.893* 0.928* 0.908* 0.858*
DPPH 1 0.916* 0.903* 0.823*
ABTS 1 0.924* 0.790*
FRAP 1 0.853*
RB 1
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TPC total phenolic content, ABTS ABTS radical scavenging capacity, DPPH DPPH radical scavenging capacity, FRAP ferric-reducing antioxidant power, RB assay Singlet oxygen scavenging capacity (*P < 0.01)

In conclusion, antioxidant capacity including singlet oxygen scavenging activity was investigated in 54 medicinal plants from Nepal. Among the 54 plant extracts, P. capitata, E. marginatum and E. acuminata showed a strong antioxidant activity. Readings from four antioxidant capacity assays (RB, DPPH, ABTS and FRAP) showed a high correlation (r ≥ 0.858) with TPC. In addition, singlet oxygen scavenging capacity using RB and TMB showed good correlation (r ≥ 0.790) with TPC including other antioxidant capacities. Therefore, this study suggests a novel and reliable approach for evaluating the singlet oxygen scavenging capacity. In vitro and in vivo studies on P. capitata, E. marginatum and E. acuminata are needed for further understanding of their bioactivities.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 23 kb) (23.7KB, docx)

Acknowledgements

The authors acknowledge the medicinal plant extracts in Nepal provided from the Ethnobotanical Society of Nepal, and Central Department of Biotechnology, Tribhuvan University, Kathmandu (Nepal). This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No. 2022R1C1C10117701161782064340101) and the National Research Foundation of Korea (NRF) funded by the Mistry of Education267 (2021R1A6A1A03039211).

Declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Footnotes

Publisher's Note

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Contributor Information

Chan Seo, Email: opp8453@gmail.com.

Hyun Woo An, Email: zksxmsmsla@naver.com.

Won Han, Email: hanwon0427@naver.com.

Joo Won Lee, Email: moveone1995@naver.com.

Krishna K. Shrestha, Email: kkshrestha123@gmail.com

Won-Kyo Jung, Email: wkjung@pknu.ac.kr.

Joong Ho Shin, Email: jhshin@pknu.ac.kr.

Sang Gil Lee, Email: sglee1125@pknu.ac.kr.

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