Phenolic compounds from Citrus leaves: antioxidant activity and enzymatic browning inhibition
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,
Abstract
Background
Phenolic compounds from Citrus are known to be a topic of many studies due to their biological properties including antioxidant activity.
Methods
Methanolic and aqueous extracts were isolated from Citrus leaves of different species (C. clementina, C. limon, C. hamlin, C. navel, C. aurantifolia, C. aurantium and C. grandis) harvested in Algeria.
Results
The results showed that aqueous extracts of all species are rich in total phenolic compounds and flavonoids (from 68.23 to 125.28 mg GAE/g DM) and (from 11.99 to 46.25 mg QE/g DM) respectively. The methanolic and aqueous extracts were examined for in vitro antioxidant properties using various antioxidant assays. For aqueous extracts, C. limon showed an important DPPH radical scavenging activity (IC50 35.35 µg/mL), and C. clementina exerted the highest ABTS radical scavenging activity (1,174.43 µM ET/g DM) and a significant ferric reducing potential (30.60 mg BHAE/g DM). For methanolic extracts, C. clementina showed the highest antioxidant activity for all the realized assays (IC50 41.85 µg/mL, 378.63 µM ET/g DM and 13.85 mg BHAE/g DM) for DPPH, ABTS radicals scavenging activities and ferric reducing potential respectively. Antiperoxidase and antipolyphenol oxidase activities of these samples were also evaluated.
Conclusions
In this investigation, the assessment of antiperoxidase activity proved that the leaves extracts of different species were able to inhibit peroxidase activity. However, this inhibition varied with the species and the source of these enzymes. On the other hand, the aqueous extracts of different species showed moderate inhibition of polyphenol oxidase, while no effect on these enzymes was obtained with methanolic extracts.
Acknowledgments
The authors are thankful to the members of the Faculty of Natural Sciences and Life, and the Plant Biotechnology & Ethnobotany laboratory, University of Bejaia, Algeria.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
References
1. Koechlin-Ramonatsco C. Oxygen, oxidative stress and antioxidant supplementation, or another way for nutrition in respiratory diseases. Nutr Clin Metab 2006;20:165–177.10.1016/j.nupar.2006.10.178Search in Google Scholar
2. Baudin B. Stress oxydant et pathologies cardiovasculaires. Mt Cardio 2006;2:43–52.Search in Google Scholar
3. Hannebelle T, Sahpaz S, Bailleul F. Polyphénols végétaux, sources, utilisation et potentiel dans la lutte contre le stress oxydatif. Phytothérapie 2004;1:3–6.10.1007/s10298-004-0003-8Search in Google Scholar
4. Iserin P, Massou M, Restellini JP, Moulard F, Zha E, Delarouque R. Encyclopédie des plantes médicinales 2001;4.Search in Google Scholar
5. Vámos-Vigyázó L. Polyphenol oxidase and peroxidase in fruits and vegetables. CRC Crit Rev Food Sci Nutr 1981;15:49–127.10.1080/10408398109527312Search in Google Scholar PubMed
6. Lee CY, Whitaker JR. Enzymatic browning and its prevention (ACS Symposium Series). Washington, DC: American Chemical Society, 1995.10.1021/bk-1995-0600Search in Google Scholar
7. Marusak CM, Trobaugh NM, Flurkey WH, Inlow JK. Comparative analysis of polyphenol oxidase from plant and fungal species. J Inorg Biochem 2006;100:108–123.10.1016/j.jinorgbio.2005.10.008Search in Google Scholar PubMed
8. Gawlik-Dziki U, Szymanowska U, Baraniak B. Characterization of polyphenol oxidase from broccoli (Brassica oleracea var. Botrytis italica) florets. Food Chem 2007;105:1047–1053.10.1016/j.foodchem.2007.05.012Search in Google Scholar
9. Baaziz M, Qacif N, Bendiab K, Aouad A. Les Peroxydases des plantes. Aspect théorique et Applications pratiques. Enzymol Métab 2006;:17–20.Search in Google Scholar
10. Nicoli MC, Elizalde BE, Pitotti A, Lerici CR. Effect of sugars and Maillard reaction products on polyphenol oxidase and peroxidase activity in food. J Food Biochem 1991;15:169–184.10.1111/j.1745-4514.1991.tb00153.xSearch in Google Scholar
11. Kim MJ, Kim CY, Park I. Prevention of enzymatic browning of pear by onion extract. Food Chem 2005;89:181–184.10.1016/j.foodchem.2004.02.018Search in Google Scholar
12. FAO. Statistical Databases. 2012 Accessed 19 July 2013 Available at: www.FAO.org.Search in Google Scholar
13. Aruoma AO. Extracts as antioxidant prophylactic agents. Inform 1997;8:1236–1242.Search in Google Scholar
14. Kamran G, Youcef G, Ebrahimzadeh MA. Antioxidant activity, phenol and flavonoid contents of 13 Citrus species peels and tissues. Pak J Pharm Sci 2009;22:277–281.Search in Google Scholar
15. Ma YQ, Chen JC, Liu DH, Ye XQ. Simultaneous extraction of phenolic com-pounds of Citrus peel extracts: effect of ultrasound. Ultrason Sonochem 2009;16:57–62.10.1016/j.ultsonch.2008.04.012Search in Google Scholar PubMed
16. Falleh H, Ksouri R, Chaieb K, Karray-Bouraoui N, Trabelsi N, Boulaaba M. Phenolic composition of Cynara cardunculus L. organs, and their biological activities. C R Biol 2008;331:372–379.10.1016/j.crvi.2008.02.008Search in Google Scholar PubMed
17. Perez YY, Jimenez-Ferrer E, Alonso D, Botello-Amaro CA, Zamilpa A. Citrus limetta leaves extract antagonizes the hypertensive effect of angiotensin II. J Ethnopharm 2010;128:611–614.10.1016/j.jep.2010.01.059Search in Google Scholar PubMed
18. Coe S, Fraser A, Ryan L. Polyphenol bioaccessibility and sugar reducing capacity of black green, and white teas. Int J Food Sci 2013;2013:1–6.10.1155/2013/238216Search in Google Scholar
19. Kadri N, Khettal B, Aid Y, Kherfellah S, Sobhi W, Barragan-Montero V. Some physicochemical characteristics of pinus (Pinus halepensis Mill., Pinus pinea L., Pinus pinaster and Pinus canariensis) seeds from North Algeria, their lipid profiles and volatile contents. Food Chem 2015;188:184–192.10.1016/j.foodchem.2015.04.138Search in Google Scholar
20. Brand-Williams W, Cuvelier M, Berset C. Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci Technol 1995;28:25–30.10.1016/S0023-6438(95)80008-5Search in Google Scholar
21. Masuda T, Yonemori S, Oyama Y, Takeda Y, Tanaka T, Andoh T. Evaluation of the antioxidant activity of environmental plants: activity of the leaf extracts from seashore plants. J Agri Food Chem 1999;47:1749–1754.10.1021/jf980864sSearch in Google Scholar
22. Lien E, Sellati TJ, Yoshimura A, Flo TH, Rawadi G, Finberg RW. Toll-like receptor 2 functions as a pattern recognition receptor for diverse bacterial products. J Biol Chem 1999;274:33419–33425.10.1074/jbc.274.47.33419Search in Google Scholar
23. Van Den Berg R, Haenen GR, Van Den Berg H, Bast A. Applicability of an improved Trolox equivalent antioxidant capacity (TEAC) assay for evaluation of antioxidant capacity measurements of mixtures. Food Chem 1999;66:511–517.10.1016/S0308-8146(99)00089-8Search in Google Scholar
24. Amarowicz R, Pegg R, Rahimi-Moghaddam P, Barl B, Weil J. Free radical scavenging capacity and antioxidant activity of selected plant species from the Canadian prairies. Food Chem 2004;84:551–562.10.1016/S0308-8146(03)00278-4Search in Google Scholar
25. Ponce AG, Del Valle CE, Roura SI. Natural essential oils as reducing agents of peroxidase activity in leafy vegetables. LWT-Food Sci Technol 2004;37:199–204.10.1016/j.lwt.2003.07.005Search in Google Scholar
26. Lee MY, Lee MK, Park I. Inhibitory effect of onion extract on polyphenol oxidase and enzymatic browning of taro (Colocasia antiquorum var. esculenta. Food Chem 2007;10:528–532.10.1016/j.foodchem.2007.04.010Search in Google Scholar
27. Roginsky V, Lissi EA. Review of methods to determine chain-breaking antioxidant activity in food. Food Chem 2005;92:235–254.10.1016/j.foodchem.2004.08.004Search in Google Scholar
28. Muthiah P, Umamaheswari M, Asokkumar K. In vitro antioxidant activities of leaves, fruits and peel extracts of Citrus. Int J Phytopharm 2012;2:13–20.10.7439/ijpp.v2i1.293Search in Google Scholar
29. Tawaha K, Alali FQ, Gharaibeh M, Mohammad M, El-Elimat T. Antioxidant activity and total phenolic content of selected Jordanian plant species. Food Chem 2007;104:1372–1378.10.1016/j.foodchem.2007.01.064Search in Google Scholar
30. Menichini F, Loizzo MR, Bonesi M, Conforti F, De Luca D, Statti GA. Phytochemical profile, antioxidant, antiinflammatory and hypoglycemic potential of hydroalcoholic extracts from Citrus medica L. cv Diamante flowers, leaves and fruits at two maturity stages. Food Chem Toxicol 2011;49:1549–1555.10.1016/j.fct.2011.03.048Search in Google Scholar
31. Kammoun BA, Boudhrioua MN, Kechaou N. Moisture sorption isotherms experimental and mathematical investigations of orange (Citrus sinensis) peel and leaves. Food Chem 2012;132:1728–1735.10.1016/j.foodchem.2011.06.059Search in Google Scholar
32. Bougandoura N, Bendimerad N. Evaluation de l’activité antioxydante des extraits aqueux et méthanoliques de Satureja calamintha ssp. Nepeta (L.) Briq. Revue «Nature & Technologie» B-Sciences Agronomiques et Biologiques 2012;9:14–19.Search in Google Scholar
33. Abd Ghafar MF, Nagendra M, Prasad K, Weng KK, Ismail A. Flavonoid, hesperidine, total phenolic contents and antioxidant activities from Citrus species. Afr J Biotechnol 2010;9:326–330.Search in Google Scholar
34. Makkar HPS, Singh B, Dawra RK. Effect of tannins rich leaves of oak (Quercus incana) on various microbial enzyme activities of the bovin rumen. Brit J Nutr 1988;60:287–296.10.1079/BJN19880100Search in Google Scholar
35. Sharma RR, Goswami AM, Singh CN, Chhonkar OP, Singh G. Catecholase and cresolase activities and phenolic content in mango (Mangifera indica L.) at panicle initiation. Sci Hortic 2001;87:147–151.10.1016/S0304-4238(00)00170-9Search in Google Scholar
36. Kong KW, Khoo HE, Prasad KN, Ismail A, Tan CP, Rajab NF. Revealing the power of the natural red pigment lycopene. Molecules 2010;15:959–987.10.3390/molecules15020959Search in Google Scholar PubMed PubMed Central
37. Jabri-Karoui I, Marzouk B. Characterization of bioactive compounds in Tunisian bitter orange (Citrus aurantium L.) Peel and juice and determination of their antioxidant activities. Biomed Res Int 2013;2013:1–12.10.1155/2013/345415Search in Google Scholar PubMed PubMed Central
38. Xu G, Ye X, Liu D, Ma Y, Chen J. Composition and distribution of phenolic acids in Ponkan (Citrus poonensis Hort. ex Tanaka) and Huyou (Citrus paradisi Macf. J Food Compos Anal 2008;21:382–389. Changshanhuyou) during maturity.10.1016/j.jfca.2008.03.003Search in Google Scholar
39. Karimi E, Oskoueian E, Hendra R, Oskoueian A, Jaafar HZE. Phenolic compounds, characterization and biological activities of Citrus aurantium bloom. Molecules 2012;17:1203–1218.10.3390/molecules17021203Search in Google Scholar PubMed PubMed Central
40. De Pooter HL, Schamp N. Comparison of the volatile composition of some Calamintha satureja species. Brunk EJ, editors. Progress in essential oil research. Berlin: Walter De Gruyter, 1986.Search in Google Scholar
41. Bourgou S, Ksouri R, Bellila A, Skandrani I, Falleh H, Marzouk B. Phenolic composition and biological activities of Tunisian Nigella sativa L. shoots and & roots. C R Biol 2008;331:48–55.10.1016/j.crvi.2007.11.001Search in Google Scholar PubMed
42. Naczk M, Shahidi F. Extraction and analysis of phenolics in food. J Chromatogr A 2004;1054:95–111.10.1016/S0021-9673(04)01409-8Search in Google Scholar
43. Moure A, Cruz JM, Franco D, Dominguez JM, Sineiro J, Dominguez H. Natural antioxidants from residual sources. Food Chem 2001;72:145–171.10.1016/S0308-8146(00)00223-5Search in Google Scholar
44. Djeridane A, Yousfi M, Nadjemi B, Boutassouna D, Stocker P, Vidal N. Antioxidant activity of some Algerian medicinal plants extracts containing phenolic compounds. Food Chem 2006;97:654–660.10.1016/j.foodchem.2005.04.028Search in Google Scholar
45. Olszewska MA, Presler A, Michel P. Profiling of phenolic compounds and antioxidant activity of dry extracts from the selected Sorbus species. Molecules 2012;17:3093–3113.10.3390/molecules17033093Search in Google Scholar
46. Zou Y, Lu Y, Wei D. Antioxidant activity of a flavonoid rich extract of Hypericum perforatum L. In vitro. J Agri Food Chem 2004;52:5032–5039.10.1021/jf049571rSearch in Google Scholar
47. Lagha-Benamrouche S, Madani K. Phenolic contents and antioxidant activity of orange varieties (Citrus sinensis L. and Citrus aurantium L.) cultivated in Algeria: Peels and leaves. Ind Crops Prod 2013;50:723–730.10.1016/j.indcrop.2013.07.048Search in Google Scholar
48. Floegel A, Kim D, Chung S, Koo SI, Chun OK. Comparison of ABTS/DPPH assays to measure antioxidant capacity in popular antioxidant-rich US foods. J Food Compos Anal 2011;24:1043–1048.10.1016/j.jfca.2011.01.008Search in Google Scholar
49. Heim KE, Tagliaferro AR, Bobilya DJ. Flavonoid antioxidants: chemistry, metabolism and structure-activity relationship. J Nutr Biochem 2002;13:572–584.10.1016/S0955-2863(02)00208-5Search in Google Scholar
50. Zheng W, Wang SY. Antioxidant activity and phenolic compounds in selected herbs. J Agri Food Chem 2001;49:5165–5170.10.1021/jf010697nSearch in Google Scholar PubMed
51. Hayes JE, Allena P, Bruntona N, O’Grady MN, Kerry JP. Phenolic composition and in vitro antioxidant capacity of four commercial phytochemical products: Olive leaf extract (Olea europaea L.), lutein, sesamol and ellagic acid. Food Chem 2011;126:948–955.10.1016/j.foodchem.2010.11.092Search in Google Scholar
52. Singh N, Rajini PS. Free radical scavenging activity of an aqueous extract of potato peel. Food Chem 2004;85:611–616.10.1016/j.foodchem.2003.07.003Search in Google Scholar
53. Calabro ML, Galtieri V, Cutroneo P, Tommasini S, Ficarra P, Ficarra R. Study of the extraction procedure by experimental design and validation of a LC method for determination of flavonoids in Citrus bergamia juice. J Pharmaceut Biomed 2004;35:349–363.10.1016/S0731-7085(03)00585-5Search in Google Scholar
54. Jayaprakasha GK, Girennavar B, Patil BS. Antioxidant capacity of pummelo and navel oranges: extraction efficiency of solvents in sequence. LWT-Food Sci Technol 2008;41:376–384.10.1016/j.lwt.2007.03.017Search in Google Scholar
55. Alikhani M, Sharifani M, Mousavizadeh SJ, Azizi M. The antioxidative activity of some essential oils in reducing peroxidase activity and enzymatic browning in some vegetables. J Agric Sci Nat Resour 2009;16:203–207.Search in Google Scholar
56. Mousavizadeh SJ, Sedaghathoor S, Khorami H. Essential oils as reducing agents of cabbage peroxidase. Sci Hortic 2011;128:388–392.10.1016/j.scienta.2011.01.027Search in Google Scholar
57. Shannon IM, Kay E, Lew JY. Peroxidase isoenzymes from horseradish rots. Isolation and physical properties. J Biol Chem 1996;241:2166–2172.10.1016/S0021-9258(18)96680-9Search in Google Scholar
58. Lee HC, Klein BP. Evaluation of combined effects of heat treatment and antioxidant on peroxidase activity of crude extract of green peas. Food Chem 1989;32:151–158.10.1016/0308-8146(89)90136-2Search in Google Scholar
59. Espin JC, Garcia-Ruiz PA, Tudela J, Varon R, Garcia-Canovas F. Monophenolase and diphenolase reaction mechanisms of apple and pear polyphenol oxidases. J Agr Food Chem 1998;46:2968–2975.10.1021/jf971045vSearch in Google Scholar
60. Jang MS, Sanada A, Ushio H, Tanaka M, Ohshima T. Inhibitory effects of ‘Enokitake’ mushroom extracts on polyphenol oxidase and prevention of apple browning. LWT-Food Sci Technol 2002;35:697–702.10.1006/fstl.2002.0937Search in Google Scholar
61. Shmitz GE, Sullivan ML, Hatfield RD. Three polyphenol oxidases from red clover (Trifolium pratense) differ in enzymatic activities and activation properties. J Agri Food Chem 2008;56:272–280.10.1021/jf072488uSearch in Google Scholar PubMed
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Articles in the same Issue
- Review
- Herbal approach in the treatment of pancytopenia
- Medical Education
- Attitudes, skill and use of evidence-based practice among US Western herbal medicine providers: a national survey
- Naturopaths in Ontario, Canada: geographic patterns in intermediately-sized metropolitan areas and integration implications
- Preclinical Studies
- Effects of luteolin and luteolin-morphine co-administration on acute and chronic pain and sciatic nerve ligated-induced neuropathy in mice
- In vivo analgesic, antipyretic and anti-inflammatory potential of leaf extracts and fractions of Eria javanica
- Modulatory effects of melatonin and vitamin C on oxidative stress-mediated haemolytic anaemia and associated cardiovascular dysfunctions in rats
- Phenolic compounds from Citrus leaves: antioxidant activity and enzymatic browning inhibition
- Berberis vulgaris L. effects on oxidative stress and liver injury in lead-intoxicated mice
- Organo-protective and antioxidant properties of leaf extracts of Syzygium guineense var macrocarpum against ferric nitriloacetate-induced stress of Wistar rats
- Clinical Studies
- Acupuncture decreases competitive anxiety prior to a competition in young athletes: a randomized controlled trial pilot study
- Case Report
- Herbal and dietary supplements related to diarrhea and acute kidney injury: a case report
Articles in the same Issue
- Review
- Herbal approach in the treatment of pancytopenia
- Medical Education
- Attitudes, skill and use of evidence-based practice among US Western herbal medicine providers: a national survey
- Naturopaths in Ontario, Canada: geographic patterns in intermediately-sized metropolitan areas and integration implications
- Preclinical Studies
- Effects of luteolin and luteolin-morphine co-administration on acute and chronic pain and sciatic nerve ligated-induced neuropathy in mice
- In vivo analgesic, antipyretic and anti-inflammatory potential of leaf extracts and fractions of Eria javanica
- Modulatory effects of melatonin and vitamin C on oxidative stress-mediated haemolytic anaemia and associated cardiovascular dysfunctions in rats
- Phenolic compounds from Citrus leaves: antioxidant activity and enzymatic browning inhibition
- Berberis vulgaris L. effects on oxidative stress and liver injury in lead-intoxicated mice
- Organo-protective and antioxidant properties of leaf extracts of Syzygium guineense var macrocarpum against ferric nitriloacetate-induced stress of Wistar rats
- Clinical Studies
- Acupuncture decreases competitive anxiety prior to a competition in young athletes: a randomized controlled trial pilot study
- Case Report
- Herbal and dietary supplements related to diarrhea and acute kidney injury: a case report
