Theoretical study of the antioxidant capacity of the flavonoids present in the Annona muricata (Soursop) leaves

  • María F. Manrique-de-la-Cuba
  • Pamela Gamero-Begazo
  • Diego E. Valencia
  • Haruna L. Barazorda-Ccahuana
  • Badhin GómezEmail author
Original Paper
Part of the following topical collections:
  1. QUITEL 2018 (44th Congress of Theoretical Chemists of Latin Expression)


A theoretical approach was used to evaluate the antioxidant capacity of 20 flavonoids reported in Annona muricata leaves. The theoretical study was at the GGA level using the wB97XD functional and the cc-pvtz basis set. The calculations were performed in gas phase and implicit solvent phase. The flavonol robinetin (03c) and the flavanol gallocatechin (01c) are species that exhibited the best antioxidant capacity in the HAT, SEPT, and SPLET mechanisms. On the other hand, in the SET I mechanism, flavonol quercetin (03b) was the best, and in the SET II mechanism, the most favored species is the flavanol catechin (01a). However, these species do not achieve to overcome the antioxidant capacity presented by the Trolox.


GGA DFT Flavonoids Annona muricata Soursop HAT SEPT SPLET SET 



The authors acknowledge the Vice-Rectorate for Research of the Universidad Católica de Santa María for the financial support through the internal project 24975-R-2017.


  1. 1.
    Carocho M, Ferreira IC (2013) A review on antioxidants, prooxidants and related controversy: natural and synthetic compounds, screening and analysis methodologies and future perspectives. Food Chem Toxicol 51:15–25CrossRefGoogle Scholar
  2. 2.
    Uttara B, Singh AV, Zamboni P, Mahajan R (2009) Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 7:65–74CrossRefGoogle Scholar
  3. 3.
    Aruoma OI (1998) Free radicals, oxidative stress, and antioxidants in human health and disease. J Am Oil Chem Soc 75:199–212CrossRefGoogle Scholar
  4. 4.
    Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194CrossRefGoogle Scholar
  5. 5.
    Rahal A, Kumar A, Singh V, Yadav B, Tiwari R, Chakraborty S, Dhama K (2014) Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int 2014:1–19CrossRefGoogle Scholar
  6. 6.
    Shahreza FD (2017) Oxidative stress, free radicals, kidney disease and plant antioxidants. Immunopathol Persa 3:1–6Google Scholar
  7. 7.
    Iuga C, Alvarez-Idaboy JR, Russo N (2012) Antioxidant activity of trans-resveratrol toward hydroxyl and hydroperoxyl radicals: a quantum chemical and computational kinetics study. J Org Chem 77:3868–3877CrossRefGoogle Scholar
  8. 8.
    Procházková D, Bouṡová I, Wilhelmová N (2011) Antioxidant and prooxidant properties of flavonoids. Fitoterapia 82:513–523CrossRefGoogle Scholar
  9. 9.
    Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 97:55–74CrossRefGoogle Scholar
  10. 10.
    Gülċin I (2012) Antioxidant activity of food constituents: an overview. Arch Toxicol 86:345–391CrossRefGoogle Scholar
  11. 11.
    Rao V, Balachandran B, Shen H, Logan A, Rao L (2011) In vitro and in vivo antioxidant properties of the plant-based supplement greens+. Int J Mol Sci 12:4896–4908CrossRefGoogle Scholar
  12. 12.
    Moghadamtousi S, Fadaeinasab M, Nikzad S, Mohan G, Ali H, Kadir H (2015) Annona muricata (Annonaceae): a review of its traditional uses, isolated acetogenins and biological activities. Int J Mol Sci 16:15625–15658CrossRefGoogle Scholar
  13. 13.
    Coria-Téllez A V, Montalvo-Gónzalez E, Yahia EM, Obledo-Vázquez E N (2018) Annona muricata: a comprehensive review on its traditional medicinal uses, phytochemicals, pharmacological activities, mechanisms of action and toxicity. Arab J Chem 11:662–691CrossRefGoogle Scholar
  14. 14.
    Usunomena U, Paulinus ON (2015) Phytochemical analysis and mineral composition of Annona muricata leaves. IJRCD 1:38–42Google Scholar
  15. 15.
    Correa J, Ortiz D, Larrahondo J, Sanchez M, Pachon H (2012) Actividad antioxidante en guanábana (Annona muricata l.): una revisión bibliográfica. Bol latinoam Caribe plantas med aromát 11:111–126Google Scholar
  16. 16.
    George VC, Kumar DN, Suresh P, Kumar RA (2015) Antioxidant, DNA protective efficacy and HPLC analysis of Annona muricata (Soursop) extracts. J Food Sci Technol 52:2328–2335CrossRefGoogle Scholar
  17. 17.
    Agu KC, Okolie PN (2017) Proximate composition, phytochemical analysis, and in vitro antioxidant potentials of extracts of Annona muricata (Soursop). Food Sci Nutr 5:1029–1036CrossRefGoogle Scholar
  18. 18.
    Muthu S, Durairaj B (2015) Evaluation of antioxidant and free radical scavenging activity of Annona muricata. Euro J Exp Bio 5:39–45Google Scholar
  19. 19.
    Sujayil T, Dhanaraj T (2016) Determination of bioactive compounds in Evolvulus alsinoides leaf extract using GC-MS technique. Res J Life Sci Bioinform Pharm Chem Sci 2:34–38Google Scholar
  20. 20.
    Syed Najmuddin S, Alitheen N, Hamid M, Nik Abd Rahman N (2017) Comparative study of antioxidant level and activity from leaf extracts of Annona muricata Linn obtained from different locations. Pertanika J Trop Agric Sci 40:119–130Google Scholar
  21. 21.
    Xiao J (2017) Dietary flavonoid aglycones their glycosides: which show better biological significance. Crit Rev Food Sci Nutr 57:1874–1905PubMedGoogle Scholar
  22. 22.
    Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2:53CrossRefGoogle Scholar
  23. 23.
    Schäffner A R (2016) Flavonoid biosynthesis and Arabidopsis genetics: more good music. J Exp Bot 67:1203–1204CrossRefGoogle Scholar
  24. 24.
    McIntosh CA, Owens DK (2016) Advances in flavonoid glycosyltransferase research: integrating recent findings with long-term citrus studies. Phytochem Rev 15:1075–1091CrossRefGoogle Scholar
  25. 25.
    Heim KE, Tagliaferro AR, Bobilya DJ (2002) Flavonoid antioxidants: chemistry, metabolism and structure–activity relationships. J Nutr Biochem 13:572–584CrossRefGoogle Scholar
  26. 26.
    De Beer D, Joubert E, Gelderblom W, Manley M (2002) Phenolic compounds: a review of their possible role as in vivo antioxidants of wine. S Afr J Enol Vitic 23:48–61Google Scholar
  27. 27.
    Xiao J, Capanoglu E, Jassbi AR, Miron A (2016) Advance on the flavonoid C-glycosides and health benefits. Crit Rev Food Sci Nutr 56:S29—S45Google Scholar
  28. 28.
    de Souza GL, de Oliveira LM, Vicari RG, Brown A (2016) A DFT investigation on the structural and antioxidant properties of new isolated interglycosidic O-(1→3) linkage flavonols. J Mol Model 22:100CrossRefGoogle Scholar
  29. 29.
    Yang D, Xie H, Jia X, Wei X (2015) Flavonoid C-glycosides from star fruit and their antioxidant activity. J Funct Foods 16:204–210CrossRefGoogle Scholar
  30. 30.
    Jiménez V M, Gruschwitz M, Schweiggert RM, Carle R, Esquivel P (2014) Identification of phenolic compounds in Soursop (Annona muricata) pulp by high-performance liquid chromatography with diode array and electrospray ionization mass spectrometric detection. Int Food Res 65:42–46CrossRefGoogle Scholar
  31. 31.
    Weston LA, Mathesius U (2013) Flavonoids: their structure, biosynthesis and role in the rhizosphere, including allelopathy. J Chem Ecol 39:283–297CrossRefGoogle Scholar
  32. 32.
    Zhang D, Liu Y, Chu L, Wei Y, Wang D, Cai S, Zhou F, Ji B (2013) Relationship between the structures of flavonoids and oxygen radical absorbance capacity values: a quantum chemical analysis. J Phys Chem A 117:1784–1794CrossRefGoogle Scholar
  33. 33.
    Pietta P-G (2000) Flavonoids as antioxidants. J Nat Prod 63:1035–1042CrossRefGoogle Scholar
  34. 34.
    Kabanda MM, Mammino L, Murulana LC, Mwangi HM, Mabusela WT (2015) Antioxidant radical scavenging properties of phenolic pent-4-en-1-yne derivatives isolated from Hypoxis rooperi. A DFT study in vacuo and in solution. Int J Food Prop 18:149–164CrossRefGoogle Scholar
  35. 35.
    Sebastian RS, Enns CW, Goldman JD, Steinfeldt LC, Martin CL, Clemens JC, Murayi T, Moshfegh AJ (2017) New, publicly available flavonoid data products: valuable resources for emerging science. J Food Compost Anal 64:68–72CrossRefGoogle Scholar
  36. 36.
    Ivey KL, Jensen MK, Hodgson JM, Eliassen AH, Cassidy A, Rimm EB (2017) Association of flavonoid-rich foods and flavonoids with risk of all-cause mortality. Br J Nutr 117:1470–1477CrossRefGoogle Scholar
  37. 37.
    Galano A, Mazzone G, Alvarez-Diduk R, Marino T, Alvarez-Idaboy JR, Russo N (2016) Food antioxidants: chemical insights at the molecular level. Annu Rev Food Sci Technol 7:335–352CrossRefGoogle Scholar
  38. 38.
    Amić D, Stepanić V, Luċić B, Marković Z, Marković JMD (2013) PM6 study of free radical scavenging mechanisms of flavonoids: why does O–H bond dissociation enthalpy effectively represent free radical scavenging activity. J Mol Model 19:2593– 2603CrossRefGoogle Scholar
  39. 39.
    Galano A (2015) Free radicals induced oxidative stress at a molecular level: the current status, challenges and perspectives of computational chemistry based protocols. J Mex Chem Soc 59:231–262Google Scholar
  40. 40.
    Izadyar M, Kheirabadi RA (2016) theoretical study on the structure-radical scavenging activity of some hydroxyphenols. Phys Chem Res 4:73–82Google Scholar
  41. 41.
    Zheng Y-Z, Deng G, Liang Q, Chen D-F, Guo R, Lai R-C (2017) Antioxidant activity of quercetin and its glucosides from propolis: a theoretical study. Sci Rep 7:7543CrossRefGoogle Scholar
  42. 42.
    Shahidi F, Zhong Y (2015) Measurement of antioxidant activity. J Funct Foods 18:757–781CrossRefGoogle Scholar
  43. 43.
    Prior RL (2015) Oxygen radical absorbance capacity (ORAC): new horizons in relating dietary antioxidants/bioactives and health benefits. J Funct Foods 18:797–810CrossRefGoogle Scholar
  44. 44.
    Om A, Kim JA (2008) quantitative structure–activity relationship model for radical scavenging activity of flavonoids. J Med Food 11:29–37CrossRefGoogle Scholar
  45. 45.
    Amić D, Luċić B, Kovaċević G, Trinajstić N (2009) Bond dissociation enthalpies calculated by the PM3 method confirm activity cliffs in radical scavenging of flavonoids. Mol Divers 13:27–36CrossRefGoogle Scholar
  46. 46.
    López-Munguía A, Hernández-Romero Y, Pedraza-Chaverri J, Miranda-Molina A, Regla I, Martínez A, Castillo E (2011) Phenylpropanoid glycoside analogues: enzymatic synthesis, antioxidant activity and theoretical study of their free radical scavenger mechanism. PLoS One 6:11–18CrossRefGoogle Scholar
  47. 47.
    Primas H (2013) Chemistry, quantum mechanics and reductionism: perspectives in theoretical chemistry; Springer Science & Business Media, vol. 24Google Scholar
  48. 48.
    Cramer CJ (2013) Essentials of computational chemistry: theories and models. Wiley, New YorkGoogle Scholar
  49. 49.
    Lewars EG (2010) Computational chemistry: introduction to the theory and applications of molecular and quantum mechanics. Springer Science & Business Media, BerlinGoogle Scholar
  50. 50.
    Young D (2004) Computational chemistry: a practical guide for applying techniques to real-world problems. Wiley, New YorkGoogle Scholar
  51. 51.
    Jensen F (2017) Introduction to computational chemistry. Wiley, New YorkGoogle Scholar
  52. 52.
    Leach AR (2001) Molecular modelling: principles and applications. Prentice Hall, EnglandGoogle Scholar
  53. 53.
    Orio M, Pantazis DA, Neese F (2009) Density functional theory. Photosyn Res 102:443–453CrossRefGoogle Scholar
  54. 54.
    Ritchie TJ, McLay IM (2012) Should medicinal chemists do molecular modelling?. Drug Discov Today 17:534–537CrossRefGoogle Scholar
  55. 55.
    Mladenović M, Mihailović M, Bogojević D, Matić S, Nićiforović N, Mihailović V, Vuković N, Sukdolak S, Solujić S (2011) In vitro antioxidant activity of selected 4-hydroxy-chromene-2-one derivatives—SAR, QSAR and DFT studies. Int J Mol Sci 12:2822–2841CrossRefGoogle Scholar
  56. 56.
    Lespade L, Bercion S (2012) Theoretical investigation of the effect of sugar substitution on the antioxidant properties of flavonoids. Free Radic Res 46:346–358CrossRefGoogle Scholar
  57. 57.
    Sarkar A, Middya TR, Jana AD (2012) A QSAR study of radical scavenging antioxidant activity of a series of flavonoids using DFT-based quantum chemical descriptors–the importance of group frontier electron density. J Mol Model 18:2621–2631CrossRefGoogle Scholar
  58. 58.
    Sroka Z, żbikowska B, Hładyszowski J (2015) The antiradical activity of some selected flavones and flavonols. Experimental and quantum mechanical study. J Mol Model 21:307CrossRefGoogle Scholar
  59. 59.
    Chen Y, Xiao H, Zheng J, Liang G (2015) Structure-thermodynamics-antioxidant activity relationships of selected natural phenolic acids and derivatives: An experimental and theoretical evaluation. PLoS One 10:1–20Google Scholar
  60. 60.
    Dennington R, Keith TA, Millam JM (2016) GaussView Version 6., Semichem Inc. Shawnee Mission KSGoogle Scholar
  61. 61.
    Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Petersson GA, Nakatsuji H, Li X, Caricato M, Marenich AV, Bloino J, Janesko BG, Gomperts R, Mennucci B, Hratchian HP, Ortiz JV, Izmaylov AF, Sonnenberg JL, Williams-Young D, Ding F, Lipparini F, Egidi F, Goings J, Peng B, Petrone A, Henderson T, Ranasinghe D, Zakrzewski VG, Gao J, Rega N, Zheng G, Liang W, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Throssell K, Montgomery J A Jr., Peralta JE, Ogliaro F, Bearpark MJ, Heyd JJ, Brothers EN, Kudin KN, Staroverov VN, Keith TA, Kobayashi R, Normand J, Raghavachari K, Rendell AP, Burant JC, Iyengar SS, Tomasi J, Cossi M, Millam JM, Klene M, Adamo C, Cammi R, Ochterski JW, Martin RL, Morokuma K, Farkas O, Foresman JB, Fox DJ (2016) Gaussian 16 Revision B.01. Gaussian Inc. Wallingford CTGoogle Scholar
  62. 62.
    Dewar MJ, Zoebisch EG, Healy EF, Stewart JJ (1985) Development and use of quantum mechanical molecular models. 76. AM1: a new general purpose quantum mechanical molecular model. J Am Chem Soc 107:3902–3909CrossRefGoogle Scholar
  63. 63.
    Chai J-D, Head-Gordon M (2008) Long-range corrected hybrid density functionals with damped atom–atom dispersion corrections. Phys Chem Chem Phys 10:6615–6620CrossRefGoogle Scholar
  64. 64.
    Kendall RA, Dunning TH, Harrison RJ (1992) Electron affinities of the first-row atoms revisited. Systematic basis sets and wave functions. J Chem Phys 96:6796–6806CrossRefGoogle Scholar
  65. 65.
    Riley KE, Op’t Holt BT, Merz KM (2007) Critical assessment of the performance of density functional methods for several atomic and molecular properties. J Chem Theory Comput 3:407–433CrossRefGoogle Scholar
  66. 66.
    Marenich AV, Cramer CJ, Truhlar DG (2009) Universal solvation model based on solute electron density and on a continuum model of the solvent defined by the bulk dielectric constant and atomic surface tensions. J Phys Chem B 113:6378–6396CrossRefGoogle Scholar
  67. 67.
    Burda S, Oleszek W (2001) Antioxidant and antiradical activities of flavonoids. J Agric Food Chem 49:2774–2779CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • María F. Manrique-de-la-Cuba
    • 1
  • Pamela Gamero-Begazo
    • 1
  • Diego E. Valencia
    • 1
  • Haruna L. Barazorda-Ccahuana
    • 1
  • Badhin Gómez
    • 1
    • 2
    Email author
  1. 1.Centro de Investigación en Ingeniería Molecular – CIIM, Vicerrectorado de InvestigaciónUniversidad Católica de Santa MaríaArequipaPerú
  2. 2.Facultad de Ciencias Farmacéuticas, Bioquímicas y Biotecnológicas, Departamento de Farmacia, Bioquímica y BiotecnologíaUniversidad Católica de Santa MaríaArequipaPerú

Personalised recommendations