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. 2022 Mar 17;31(5):627–633. doi: 10.1007/s10068-022-01064-5

Antioxidant activities of premature and mature mandarin (Citrus unshiu) peel and juice extracts

Seogyeong Lee 1, Hyun Jung Kim 1,✉
PMCID: PMC9033906  PMID: 35529692

Abstract

In vitro antioxidant activities of premature and mature mandarin peel and juice extracts were investigated for their potentials as functional food materials. Total phenolic and flavonoid content of premature and mature mandarin peel and juice was in the range of 31.20 to 94.04 mg gallic acid equivalent (GAE)/g and 0.09 to 43.99 mg quercetin equivalent (QE)/g, respectively. Among flavanone compounds, hesperidin and narirutin were identified as 76.81 and 51.35 mg/g, respectively, in the premature mandarin peel extract. Mandarin peel extracts were mostly high in in vitro antioxidant activities compared to mandarin juices. Hydrogen peroxide and hydroxyl radical scavenging activities (81.52–93.24%) of the premature mandarin peel extract were higher than DPPH and ABTS+ radical scavenging activities (24.03–30.39%). These results confirmed that the potential of premature mandarin peels as a natural antioxidant source for functional foods.

Supplementary Information

The online version contains supplementary material available at 10.1007/s10068-022-01064-5.

Keywords: Premature mandarin, Mature Mandarin, Antioxidant activity, Flavanone compounds, Natural antioxidant

Introduction

With the changes in lifestyle and dietary patterns, modern people are paying attention to health foods, especially antioxidants to retard aging process and prevent lifestyle-related diseases (Khan and Dangles, 2014; Yang et al., 2018). Excessive accumulation of reactive oxygen species (ROS) including superoxide anion radical, hydroxyl radical, and hydrogen peroxide causes oxidative stress (Kim et al., 2009) with the promotion of aging and occurrence in metabolic diseases (Lee et al., 2020; Yang et al., 2018). To prevent or reduce the generation of ROS, antioxidants are commonly used in food industry and consumers are demanding natural plant-based antioxidants as well.

Mandarin is one of the most consumed fruits in the world because of its attractive color, pleasant flavors, and phytochemicals, such as phenolic acids, flavonoids, carotenoids, and vitamin C (Chen et al., 2020; Zou et al., 2016). Among 1800 species of mandarins, Citrus unshiu is the most cultivated in Jeju, Korea (Carbonell-Caballero et al., 2015; Kim and Lim, 2020a). About 50% of mandarins are processed for mandarin juice and the half of them are discarded as wastes which mostly include peel, pulp, and premature and damaged fruits (Kim and Lim, 2020a; Negro et al., 2016). Among them, mandarin peels and premature mandarins contain more health functional compounds than edible parts (Choi et al., 2019; Park et al., 2020). Flavonoids are well-known functional compounds and hesperidin, naringin, rutin, nobiletin, and tangeretin are mostly founded flavonoid compounds in mandarin (Huang et al., 2020). These flavonoids were reported to show various bioactivities, such as radical scavenging, antioxidant, and anti-inflammatory activities (Choi et al., 2019; Yi et al., 2017). Thus, mandarin flavonoids can be one of the most important bioactive compounds to reduce the generation of ROS (Yi et al., 2017). As the demand for the usage of a natural antioxidant has increased, premature mandarins which are mostly discarded during harvest can be utilized. Thus, in this study, the flavonoid compounds of premature mandarin peel and juice were analyzed and in vitro antioxidant activities were measured along with mature mandarin.

Materials and methods

Materials and chemicals

Premature mandarins (harvested from August to September, 2019) and mature (harvested in December, 2019) were purchased from a local farm (Jeju, Korea). Folin-Ciocalteu reagents, 1,1-diphenyl-2-picryl-hydrazyl (DPPH), 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) diammonium salt (ABTS), peroxidase, iron sulfate heptahydrate, and iron chloride were obtained from Sigma-Aldrich (St. Louis, MO, USA).

Preparation of premature and mature mandarin peel extract

Peels of premature and mature mandarins were separated and dried at 80 °C for 9 h. The dried peels were ground into a 40-mesh size with a blender (SMX-8000EMT, Shinil, Seoul, Korea). The powder was mixed with methanol as a ratio of 1:10 (w/v) and extracted at 50 °C for 24 h. The extract was filtered through a filter paper (Whatman No. 2, Whatman, Maidstone, UK) and methanol was evaporated using a rotary evaporator (SB-1200, EYELA, Tokyo, Japan). The concentrate was dissolved with distilled water and freeze-dried to obtain premature and mature mandarin peel powder. For the measurement of in vitro antioxidant activities, the extract was stocked in dimethyl sulfoxide (DMSO, Sigma-Aldrich) at 10 mg/mL and the stock solution was diluted accordingly.

Preparation of premature and mature mandarin juice

Premature and mature mandarin fruits after peeling off were ground using a blender (SMX-8000EMT, Shinil) to prepare mandarin juice. The juice was centrifuged at 2700 xg for 20 min (Labogene, Seoul, Korea) and the supernatant was filtered through a filter paper (Whatman). Filtered juice was freeze-dried to obtain premature and mature mandarin juice powder. For the analysis of in vitro antioxidant activities, the juice powder was stocked as described in the preparation of the peel extract.

Determination of total phenolic and flavonoid content

Total phenolic content (TPC) was determined by Folin-Ciocalteu method (Lee et al., 2020). In brief, 100 µL of a sample was mixed with 1.5 mL of distilled water and 100 µL of 2 N Folin-Ciocalteu reagent. After 30 s, 300 µL of 20% sodium carbonate was mixed and incubated at room temperature for 1 h in the dark. The absorbance was measured at 765 nm using a UV–Vis spectrophotometer (OPTIZEN 2120UV, Mecasys, Daejeon, Korea) and TPC was expressed as gallic acid equivalent (mg GAE/g of freeze-dried peel extract or juice powder).

For total flavonoid content (TFC) measurement (Yi et al., 2014), an aliquot (200 µL) was mixed with 800 µL of ethanol and 60 µL of 5% NaNO2 and incubated at room temperature for 5 min. The mixture was reacted with 60 µL of 10% AlCl3 and allowed to stand for 5 min. The 400 µL of 1 M NaOH and 500 µL of distilled water were added to the mixture. The absorbance was measured at 415 nm with UV-Vis spectrophotometer (Mecasys) and TFC was expressed as quercetin equivalent (mg QE/g of freeze-dried peel extract or juice powder).

Analysis of flavanone compounds by HPLC

Flavanone compounds were analyzed by an HPLC (Agilent 1260 series, Agilent Technologies, Santa Clara, CA, USA) with a diode array detector (G7115A DAD WR, Agilent Technologies) and a Pursuit C18 column (250 × 4.6 mm, 5 μm, Agilent Technologies) (Sun et al., 2010). Elution was performed at the flow rate of 1.0 mL/min with mobile phase consisting of 0.1% formic acid in water (solvent A) and acetonitrile (solvent B) for 0–10 min, A:B = 78:22; 10–35 min, A:B = 39:61; and 35–40 min, A:B = 0:100%. The injection volume was 20 µL and the detection wavelength was 280 nm. The chromatographic peaks of flavanone compounds were recognized by comparing retention time and UV-vis spectra of hesperidin, hesperetin, narirutin, and naringenin (Sigma-Aldrich). The flavanone contents were quantified based on the calibration curve of each standard.

In vitro antioxidant activity

DPPH radical scavenging activity was measured (Lee et al., 2020). The absorbance was measured at 517 nm using a microplate reader (Epoch™, BioTek Instruments INC., Winooski, VT, USA) after 30 min by adding 70 µL mandarin extracts or flavanone compounds into 140 µL of 1 mM DPPH solution. For ABTS+ radical scavenging activity (Sung et al., 2018), the ABTS+ radical solution was prepared by 7 mM ABTS with 2.45 mM potassium persulfate in equal quantities and allowed them to react at room temperature in the dark for 16 h. Then, 180 µL of ABTS+ radical solution was mixed with 20 µL of mandarin extracts or flavanone compounds. The absorbance was measured at 734 nm (BioTek Instruments).

Hydrogen peroxide (H2O2) scavenging activity was determined (Lee et al., 2020). Briefly, 100 µL of a sample, 20 µL of hydrogen peroxide, and 100 µL of 0.1 M phosphate buffer (pH 7.4) were mixed together and then incubated at 37 °C for 5 min. The 30 µL of 1.25 mM ABTS and 40 µL of peroxidase (1 unit/mL) were added to the mixture and incubated again at 37 °C for 10 min. The absorbance was measured at 405 nm (BioTek Instruments).

For the measurement of hydroxyl radical scavenging activity, hydroxyl radical was generated by Fenton reaction in the presence of FeSO4·7H2O (Lee et al., 2020). Two hundred µL of a sample was placed to a test tube containing 200 µL of 10 mM FeSO4·7H2O, 10 mM EDTA, 10 mM 2-deoxyribose, 10 mM hydrogen peroxide, and 1 mL of 0.1 M phosphate buffer solution (pH 7.4) and incubated at 37 °C for 2 h. After taking out 1 mL of the mixture, 1 mL of 2.8% trichloroacetic acid (TCA) and 0.4% thiobarbituric acid (TBA) solution were added and put it in a boiling water bath for 10 min. After cooling down, the absorbance was measured at 532 nm (Mecasys). All radical scavenging activities were calculated as followed: radical scavenging activity (%) = [1 − (Asample / Acontrol)] × 100 (A: absorbance at 532 nm).

Superoxide dismutase (SOD) activity were measured according to the manufacturer protocol of the SOD Assay kit (Dojindo Molecular Technologies, Inc., Tokyo, Japan). All mandarin extracts and flavanone compounds were placed to a 96-well plate and reacted with reagents in the kit. The absorbance was measured at 450 nm (BioTek Instruments).

For the reducing power (Lee et al., 2020), 1 mL of a sample, 0.1 M phosphate buffer (pH 6.6), and 1% potassium ferricyanide were mixed and incubated at 50 °C for 20 min. After the addition of 1 mL of 10% TCA, the supernatant (2 mL) from the reaction solution were mixed with 2 mL of distilled water and 400 µL of 0.1% ferric chloride and left at room temperature for 10 min. The reducing power was compared as the absorbance at 700 nm (Mecasys).

Statistical analysis

All analyses were performed in triplicate. Statistical comparisons were performed by one-way analysis of variance followed by Duncan’s multiple range test using SPSS 23.0 (SPSS Inc., Chicago, IL, USA). Significant differences were considered at p < 0.05.

Results and discussion

Total phenolic and flavonoid content of premature and mature mandarin extracts

The TPC and TFC of premature and mature mandarin peel and juice are shown in Table 1. The TPC of premature mandarin peel extract was 94.04 mg GAE/g, which was the highest. The peel extracts contained higher TPC and TFC than juices whether mandarin was premature or mature. When compared to TPC and TFC of premature and mature mandarin, premature mandarin contained greater amounts than mature did. During the maturation of mandarins, the oxidation of polyphenol by polyphenol oxidase would lead to the reduction of TPC (Dong et al., 2019). Dong et al. (2019) also reported that TPC and TFC of lemon peel was the highest in August and gradually decreased in maturing stage. The TPC in one of citrus, Yuzu was the highest in August and lowest in December (Moon et al., 2015). The results of the current study showed that mandarin peels have higher TPC and TFC than juice and premature mandarin had higher TPC and TFC than mature mandarin. Thus premature mandarin peels could be used as a good source of natural antioxidant.

Table 1.

Total phenolic and total flavonoid contents of premature and mature mandarin peel and juice

Mandarin extract Total phenolic contents1
(mg GAE/g)2 		Total flavonoid contents1
(mg QE/g) 3
Peel Premature 94.04 ± 6.25a 43.99 ± 3.73a
Mature 79.15 ± 2.38b 23.51 ± 0.81b
Juice Premature 37.05 ± 4.16c 4.20 ± 1.04c
Mature 31.20 ± 3.29c 0.09 ± 0.46d
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1Each value is mean ± standard deviation. Means with different letters in a column are significantly different at p < 0.05

2The mg GAE/g means mg gallic acid equivalent/g of freeze-dried peel extract or juice powder

3The mg QE/g means mg quercetin equivalent/g of freeze-dried peel extract or juice powder

Flavanone compounds of premature and mature mandarin extracts

Flavanone compounds, such as hesperidin, hesperetin, narirutin, and naringenin, were determined in premature and mature mandarin peel and juice extracts (Table 2). Among flavanone compounds, only hesperidin and narirutin, glycoside forms of flavanones, were detected. The concentration of hesperidin was higher than narirutin in peels. Because most flavonoids are bound to sugars by glycosidic bonds and present as glycoside forms in mandarin (Kim and Lim, 2020a), hesperetin and naringenin were not found in premature mandarin. Peels contained much greater amounts of flavanone compounds than juices, which were similar to the results of TPC and TFC (Table 1). Hesperidin and narirutin were more detected in premature mandarin than mature. The narirutin concentration in mandarin was usually high in the early stage of growing (Multari et al., 2020) and hesperidin was detected in high as well (Choi et al., 2007). In addition, hesperidin was present in high of mandarin peels while narirutin was in low (Kim and Kim, 2016). According to Chen et al. (2019), hesperidin was the most abundant flavonoid compound present in mandarin peels and flavonoid contents were different depending on the production area. Kim and Lim (2020a) reported major flavonoids of mandarin peels were hesperidin and narirutin and minor flavonoids were sinensetin, nobiletin, and tangeretin. While low quantities of naringin were found in lemon, sweet orange, and lime, hesperidin was found in high in mandarin (Khan and Dangles, 2014). These results indicated that hesperidin was the main flavonoid compound in citrus fruits and the amount and type of flavanones were depended on the species, parts, and growing stage of mandarins.

Table 2.

Flavanone compounds identified in premature and mature mandarin peel and juice

Mandarin extract Flavanone compound (mg/g)1
Hesperidin Hesperetin Narirutin Naringenin Total
Peel Premature 76.81 ± 7.32a N.D.2 51.35 ± 3.96a N.D. 128.16 ± 11.29a
Mature 62.12 ± 4.28b N.D. 24.00 ± 1.49b N.D. 86.12 ± 5.58b
Juice Premature 3.48 ± 0.20c N.D. 6.84 ± 0.30c N.D. 10.32 ± 0.50c
Mature 2.25 ± 0.01c N.D. 3.08 ± 0.01c N.D. 5.33 ± 0.01c
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1Each value is mean ± standard deviation. Means with different letters in a column are significantly different at p < 0.05

2N.D.: not detected

In vitro antioxidant activities of premature and mature mandarin extracts

In vitro antioxidant activities including DPPH radical, ABTS+ radical, hydrogen peroxide, hydroxyl radical scavenging, superoxide dismutase activity, and reducing power of premature and mature mandarin peel and juice extracts at 1 mg/mL were determined (Table 3). Additionally, the antioxidant activities of hesperidin, hesperetin, narirutin, and naringenin at 0.1 mg/mL were determined for comparison since they are known as major flavonoids in mandarin. The DPPH radical scavenging activity of premature and mature mandarin peel extract and juice was 30.39, 27.67, 26.52, and 16.74%, respectively. Hesperidin, hesperetin, narirutin, and naringenin showed 13.65, 24.95, 4.32, and 5.34% of DPPH radical scavenging activity. The ABTS+ radical scavenging activity of premature and mature mandarin peel extracts and juice was 24.91, 24.03, 8.77, and 5.82%, respectively, and that of hesperidin, hesperetin, narirutin, and naringenin was 19.49, 36.63, 2.99, and 12.12%, respectively. Mostly, the mandarin peels had higher radical scavenging activities than mandarin juices did. When comparing DPPH and ABTS+ radical scavenging activities of flavanone standards, hesperetin, an aglycone form of hesperidin was the highest and naringenin showed higher radical scavenging activity than narirutin. The glycosylation of flavanone compounds reduced the antioxidant activities compared to their aglycone forms (Di Majo et al., 2005; Wang et al., 2018).

Table 3.

In vitro antioxidant activities of premature and mature mandarin peel and juice and flavanone compounds

Sample In vitro antioxidant activity
DPPH free radical scavenging activity (%) ABTS+ radical scavenging activity (%) H2O2 scavenging activity (%) Hydroxyl radical scavenging activity (%) SOD activity (%) Reducing power (Abs)
Mandarin extract1
 Peel
  Premature 30.39 ± 1.70a2 24.91 ± 0.73a 81.52 ± 1.00b 92.74 ± 0.23a 44.31 ± 1.11a 0.93 ± 0.05a
  Mature 27.67 ± 0.99b 24.03 ± 0.77a 93.24 ± 0.43a 92.13 ± 1.24a 34.07 ± 1.31b 0.82 ± 0.03b
 Juice
  Premature 26.52 ± 1.53b 8.77 ± 0.72b 51.39 ± 2.56c 14.35 ± 1.83b 11.05 ± 0.67c 0.38 ± 0.02c
  Mature 16.74 ± 0.53c 5.82 ± 1.08c 44.90 ± 0.26d 16.84 ± 2.26b 4.87 ± 1.40d 0.23 ± 0.02d
Flavanone compound1
 Hesperidin 13.65 ± 1.03b 19.49 ± 1.38b 98.20 ± 0.17a 90.97 ± 1.23ab 25.34 ± 0.68b 0.26 ± 0.03b
 Hesperetin 24.95 ± 2.01a 36.63 ± 0.67a 96.41 ± 0.43b 90.07 ± 1.03b 33.83 ± 1.33a 0.34 ± 0.04a
 Narirutin 4.32 ± 0.39c 2.99 ± 0.07d 74.64 ± 1.02d 91.78 ± 0.78ab 25.58 ± 1.00b 0.19 ± 0.01c
 Naringenin 5.34 ± 0.37c 12.12 ± 0.12c 61.49 ± 0.63c 92.16 ± 0.67a 26.69 ± 0.44b 0.20 ± 0.01c
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1The concentration of mandarin extracts and flavanone compounds was 1 and 0.1 mg/mL, respectively

2Each value is mean ± standard deviation. Means with different letters in a column within mandarin extracts or flavanone compounds are significantly different at p < 0.05

Hydrogen peroxide (H2O2) scavenging activities of mandarin peel and juice extracts were in the range of 44.90 to 93.24% (Table 3). Peel extracts exhibited higher scavenging activity than juice. The H2O2 scavenging activities of flavanone components were in 61.49 to 98.20% and those of hesperidin and hesperetin were higher than narirutin and naringenin. Although the concentration of hesperidin and hesperetin was low at 0.1 mg/g, the H2O2 scavenging activities of hesperidin and hesperetin were similar to those of the peel extract at 10 mg/g. Moreover, Kim and Lim (2020b) reported hesperidin and narirutin separated from mandarin peels showed higher H2O2 scavenging activity than DPPH and ABTS+ radical scavenging. Similarly, in the current study, H2O2 scavenging activity of hesperidin and narirutin was higher than DPPH and ABTS+ radical scavenging activities. The H2O2 is generated from various cellular processes by oxygen molecules and relatively unreactive non-radical; however, it causes oxidative stress because it can be changed into a deleterious product, hydroxyl radical (·OH) by Fenton reaction in the presence of Fe2+. Therefore, scavenging H2O2 by antioxidants can prevent harmful reactions initiated by hydroxyl radical (Boligon et al., 2014) and premature and mature mandarin peel extracts as antioxidants effectively scavenged H2O2.

Hydroxyl radical scavenging activities of mandarin peel extracts and flavanone components were over 90%; however, those of mandarin juice were very low, 14.35 and 16.84% (Table 3). The hydroxyl radical scavenging activities of mandarin peel extracts were as high as flavanone standard components. Hayat et al. (2010) reported that the correlation between phenol content in premature mandarin pomace and hydroxyl radical scavenging activity was greater than 0.9. Additionally, the correlation between hesperidin and narirutin contents in mandarin peel extracts and hydroxyl radical scavenging activity was 0.940 and 0.787 as showing high correlation with hesperidin content (Kim and Lim, 2020b). Therefore, it is thought that mandarin peel extracts rich in hesperidin and narirutin could effectively scavenge hydroxyl radicals.

The SOD activity of premature and mature mandarin peel extracts was 44.31 and 34.07%, respectively, while that of premature and mature mandarin juice was 11.05 and 4.87%. The mandarin peels showed higher SOD activity than mandarin juices did. When compared to those of premature and mature mandarins, premature showed higher SOD activity than mature. Among flavanone compounds, hesperetin exhibited the highest SOD activity (33.83%) while other three components were in the range of 25.34–26.69%. Kim et al. (2009) study showed a high correlation between TPC and superoxide anion radical scavenging activity. In addition, Kim and Lim (2020b) reported a high correlation between hesperidin and narirutin contents and superoxide anion scavenging activity. In this study, high SOD activity in the mandarin peel extracts, which had high TPC and high concentrations of hesperidin and narirutin, were exhibited. Reducing power, which measures the transition of Fe3+ complex to Fe2+ form by reducers, indicates the electron donating capacity of the antioxidant (Sharma et al., 2018). Reducing power of mandarin peel extracts (premature 0.93 and mature 0.82) were much high compared to mandarin juices (0.38 and 0.23) and flavanone standard components (0.19–0.34) (Table 3). Similar to our results, Guimarães et al. (2010) reported mandarin peels gave better reducing power than mandarin juices.

Premature and mature mandarin peel extracts and juice, and flavanone compounds showed very high scavenging activity for hydrogen-containing radicals (H2O2 and hydroxyl radical). However, nitrogen-containing radical scavenging (DPPH and ABTS+ radical, and reducing power of Fe(CN)63−) and SOD activity were relatively low. In addition, the Fe2+ ion chelating activity was not be detected (data not shown). The structural features for efficient radical scavenging of flavonoids could be summarized: ortho-dihydroxy (catechol) structure, 2,3-double bond in conjugation with a 4-oxo functional group in the C ring, and hydroxyl groups at positions 3 and 5 (Croft, 1998; Procházková et al., 2011). The structure of flavonoids for metal ion chelating is the catechol moiety in the B ring, 3-hydroxyl and 4-oxo functional groups in the heterocyclic ring C, and 4-oxo and 5-hydroxyl groups between C and A rings (Pietta, 2000; Procházková et al., 2011). Because of the features of flavonoid structure, the metal chelating efficiencies of premature and mature mandarin peel extracts and flavanone compounds were very limited (data not shown). These results indicated that premature and mature mandarin peel extracts as antioxidants more defended hydrogen-containing radicals than nitrogen-containing radicals, superoxide anion, reducing power, or metal chelating.

Overall, the ROS scavenging activities of premature mandarin peel extract were significantly higher than mature mandarin peel extract and mandarin juice. With the results of previous studies and the current study, premature mandarin peel possibly possesses high antioxidant activities compared to mature one.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 75 KB) (275KB, docx)

Acknowledgements

This study was supported by Korean Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry through Innovational Food Technology Development Program funded by Ministry of Agriculture, Food and Rural Affairs (Grant No. 11901303).

Declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Seogyeong Lee, Email: jewel9707@naver.com.

Hyun Jung Kim, Email: hyunjkim@jejunu.ac.kr.

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