Skip to main content

Effect of in vitro gastrointestinal digestion on the total phenolic contents and antioxidant activity of wild Mediterranean edible plant extracts

European Food Research and Technology volume 245, pages 753–762 (2019)Cite this article

Abstract

The recent interest in wild edible plants is associated with their health benefits, which are mainly due to their richness in antioxidant compounds, particularly phenolics. Nevertheless, some of these compounds are metabolized after ingestion, being transformed into metabolites frequently with lower antioxidant activity. The aim of the present study was to evaluate the influence of the digestive process on the total phenolic contents and antioxidant activity of extracts from four wild edible plants used in the Mediterranean diet (Beta maritima L., Plantago major L., Oxalis pes-caprae L. and Scolymus hispanicus L.). HPLC-DAD analysis revealed that S. hispanicus is characterized by the presence of caffeoylquinic acids, dicaffeoylquinic acids and flavonol derivatives, P. major by high amounts of verbascoside, B. maritima possesses 2,4-dihydroxybenzoic acid, 5-O-caffeoylquinic acid, quercetin derivatives and kaempferol-3-O-rutinoside, and O. pes-caprae extract contains hydroxycinnamic acids and flavone derivatives. Total phenolic contents were determined by Folin–Ciocalteu assay, and antioxidant activity by the ABTS, DPPH, ORAC and FRAP assays. Phenolic contents of P. major and S. hispanicus extracts were not affected by digestion, but they significantly decreased in B. maritima after both phases of digestion process and in O. pes-caprae after the gastric phase. The antioxidant activity results varied with the extract and the method used to evaluate the activity. Results showed that P. major extract has the highest total phenolic contents and antioxidant activity, with considerable values even after digestion, reinforcing the health benefits of this species.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price includes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Hadjichambis AC, Paraskeva-Hadjichambi D, Della A, Giusti ME, De Pasquale C, Lenzarini C, Censorii E, González-Tejero MR, Sanchez-Rojas CP, Ramiro-Gutiérrez JM, Skoula M, Johnson C, Sarpaki A, Hmamouchi M, Jorhi S, El-Demerdash M, El-Zayat M, Pieroni A (2008) Wild and semi-domesticated food plant consumption in seven circum-Mediterranean areas. Int J Food Sci Nutr 59:383–414

    Article  PubMed  Google Scholar 

  2. Heinrich M, Leonti M, Nebel S, Peschel W (2005) Local food-nutraceuticals: an example of a multidisciplinary research project on local knowledge. J Physiol Pharmacol 56:5–22

    PubMed  Google Scholar 

  3. Poljuha P, Šola I, Bilić J, Dudaš S, Bilušić T, Markić J, Rusak G (2015) Phenolic composition, antioxidant capacity, energy content and gastrointestinal stability of Croatian wild edible plants. Eur Food Res Technol 241:573–585

    Article  CAS  Google Scholar 

  4. Marengo A, Maxia A, Sanna C, Bertea CM, Bicchi C, Ballero M, Cagliero C, Rubiolo P (2017) Characterization of four wild edible Carduus species from the Mediterranean region via phytochemical and biomolecular analyses. Food Res Int 100:822–831

    Article  CAS  PubMed  Google Scholar 

  5. Pinela J, Carvalho AM, Ferreira ICFR (2017) Wild edible plants: Nutritional and toxicological characteristics, retrieval strategies and importance for today’s society. Food Chem Toxicol 110:165–188

    Article  CAS  PubMed  Google Scholar 

  6. Renna M, Cocozza C, Gonnella M, Abdelrahman H, Santamaria P (2015) Elemental characterization of wild edible plants from countryside and urban areas. Food Chem 177:29–36

    Article  CAS  PubMed  Google Scholar 

  7. Sánchez-Mata MC, Cabrera Loera RD, Morales P, Fernández-Ruiz V, Cámara M, Díez Marqués C, Pardo-de-Santayana M, Tardío J (2012) Wild vegetables of the Mediterranean area as valuable sources of bioactive compounds. Genet Resour Crop Evol 59:431–443

    Article  CAS  Google Scholar 

  8. Romojaro A, Botella MA, Obón C, Pretel MT (2013) Nutritional and antioxidant properties of wild edible plants and their use as potential ingredients in the modern diet. Int J Food Sci Nutr 64:944–952

    Article  CAS  PubMed  Google Scholar 

  9. Leonti M (2012) The co-evolutionary perspective of the food-medicine continuum and wild gathered and cultivated vegetables. Genet Resour Crop Evol 59:1295–1302

    Article  Google Scholar 

  10. Rivera D, Heinrich M, Obon C, Inocencio C, Nebel S, Verde A, Fajardo J (2006) Disseminating knowledge about ‘‘local foods plants’’ and ‘‘local plant foods’’. Forum Nutr 59:75–85

    Article  PubMed  Google Scholar 

  11. Zengin G, Mahomoodally MF, Aktumsek A, Ceylan R, Uysala S, Mocan A, Yilmaz MA, Picot-Allain CMN, Ćiriće A, Glamočlija J, Soković M (2018) Functional constituents of six wild edible Silene species: a focus on their phytochemical profiles and bioactive properties. Food Biosci 23:75–82

    Article  CAS  Google Scholar 

  12. Pandey KB, Rizvi SI (2009) Plant polyphenols as dietary antioxidants in human health and disease. Oxid Med Cell Longev 2:270–278

    Article  PubMed  PubMed Central  Google Scholar 

  13. Valko M, Leibfritz D, Moncol J, Cronin MTD, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84

    Article  CAS  PubMed  Google Scholar 

  14. Niki E (2010) Assessment of antioxidant capacity in vitro and in vivo. ‎Free Radic Biol Med 49:503–515

    Article  CAS  PubMed  Google Scholar 

  15. Prior RL, Cao GH (2000) Analysis of botanicals and dietary supplements for antioxidant capacity: a review. J AOAC Int 83:950–956

    CAS  PubMed  Google Scholar 

  16. Manach C, Scalbert A, Morand C, Rémésy C, Jiménez L (2004) Polyphenols: food sources and bioavailability. Am J Clin Nutr 79:727–747

    Article  CAS  PubMed  Google Scholar 

  17. Manach C, Williamson G, Morand C, Scalbert A, Remesy C (2005) Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am J Clin Nutr 81:230S–242S

    Article  CAS  PubMed  Google Scholar 

  18. Bouayed J, Hoffman L, Bohn T (2011) Total phenolics, flavonoids, anthocyanins and antioxidant activity following simulated gastro-intestinal digestion and dialysis of apple varieties: bioaccessibility and potential uptake. Food Chem 128:14–21

    Article  CAS  PubMed  Google Scholar 

  19. Toydemir G, Capanoglu E, Kamiloglu S, Boyacioglu D, de Vos RCH, Hall RD, Beekwilder J (2013) Changes in sour cherry (Prunus cerasus L.) antioxidants during nectar processing and in vitro gastrointestinal digestion. J Funct Foods 5:1402–1413

    Article  CAS  Google Scholar 

  20. Gaspar MC, Fonseca DA, Antunes MJ, Frigerio C, Gomes NGM, Vieira M, Santos AE, Cruz MT, Cotrim MD, Campos MG (2018) Polyphenolic characterisation and bioactivity of an Oxalis pes-caprae L. leaf extract. Nat Prod Res 32:732–738

    Article  CAS  PubMed  Google Scholar 

  21. Güçlütürk I, Detsi A, Weiss EK, Ioannou E, Roussis V, Kefalas P (2012) Evaluation of anti-oxidant activity and identification of major polyphenolics of the invasive weed Oxalis pes-caprae. Phytochem Anal 23:642–646

    Article  CAS  PubMed  Google Scholar 

  22. Jarić S, Mačukanović-Jocić M, Djurdjević L, Mitrović M, Kostić O, Karadžić B, Pavlović P (2015) An ethnobotanical survey of traditionally used plants on Suva planina mountain (south-eastern Serbia). J Ethnopharmacol 175:93–108

    Article  PubMed  Google Scholar 

  23. Marmouzi I, El Karbane M, El Hamdani M, Kharbach M, Mrabti HN, Alami R, Dahraoui S, El Jemli M, Ouzzif Z, Cherrah Y, Derraji S, El Abbes Faouzi M (2017) Phytochemical and pharmacological variability in Golden Thistle functional parts: comparative study of roots, stems, leaves and flowers. Nat Prod Res 31:2669–2674

    Article  CAS  PubMed  Google Scholar 

  24. Mazzutti S, Ferreira SRS, Herrero M, Ibañez E (2017) Intensified aqueous-based processes to obtain bioactive extracts from Plantago major and Plantago lanceolata. J Supercrit Fluids 119:64–71

    Article  CAS  Google Scholar 

  25. Morales P, Ferreira ICFR, Carvalho AM, Sánchez-Mata MC, Cámara M, Fernández-Ruiz V, Pardo-de-Santayana M, Tardío J (2014) Mediterranean non-cultivated vegetables as dietary sources of compounds with antioxidant and biological activity. LWT Food Sci Technol 55:389–396

    Article  CAS  Google Scholar 

  26. Polo S, Tardío J, Vélez-del-Burgo A, Molina M, Pardo-de-Santayana M (2009) Knowledge, use and ecology of golden thistle (Scolymus hispanicus L.) in Central Spain. J Ethnobiol Ethnomed 5:42

    Article  PubMed  PubMed Central  Google Scholar 

  27. Samuelsen AB (2000) The traditional uses, chemical constituents and biological activities of Plantago major L. A review. J Ethnopharmacol 71:1–21

    Article  CAS  PubMed  Google Scholar 

  28. Ryan L, Connell OO, Sullivan O, Aherne LS, Brien ON (2008) Micellarisation of carotenoids from raw and cooked vegetables. Plant Foods Hum Nutr 63:127–133

    Article  CAS  PubMed  Google Scholar 

  29. Ainsworth EA, Gillespie KM (2007) Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nat Protoc 2:875–877

    Article  CAS  PubMed  Google Scholar 

  30. Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237

    Article  CAS  PubMed  Google Scholar 

  31. Soler-Rivas C, Espín JC, Wichers HJ (2000) An easy and fast test to compare total free radical scavenger capacity of foodstuffs. Phytochem Anal 11:330–338

    Article  CAS  Google Scholar 

  32. Gillespie KM, Chae JM, Ainsworth EA (2007) Rapid measurement of total antioxidant capacity in plants. Nat Protoc 2:867–870

    Article  CAS  PubMed  Google Scholar 

  33. Pulido R, Bravo L, Saura-Calixto F (2000) Antioxidant activity of dietary polyphenols as determined by a modified ferric reducing/antioxidant power assay. J Agric Food Chem 48:3396–340234

    Article  CAS  PubMed  Google Scholar 

  34. Hertog MGL, Hollman PCH, Katan MB, Kromhout D (1993) Intake of potentially anticarcinogenic flavonoids and their determinants in adults in The Netherlands. Nutr Cancer 20:21–29

    Article  CAS  PubMed  Google Scholar 

  35. Jacobo-Velazquez DA, Cisneros-Zevallos L (2009) Correlations of antioxidant activity against phenolic content revisited: a new approach in data analysis for food and medicinal plants. J Food Sci 74:107–113

    Article  CAS  Google Scholar 

  36. Granica S, Lohwasser U, Jöhrer K, Zidorn C (2015) Qualitative and quantitative analyses of secondary metabolites in aerial and subaerial of Scorzonera hispanica L. (black salsify). Food Chem 173:321–331

    Article  CAS  PubMed  Google Scholar 

  37. Karaköse H, Müller A, Kuhnert N (2015) Profiling and quantification of phenolics in Stevia rebaudiana leaves. J Agric Food Chem 63:9188–9198

    Article  CAS  PubMed  Google Scholar 

  38. Sareedenchai V, Zidorn C (2010) Flavonoids as chemosystematic markers in the tribe Cichorieae of the Asteraceae. Biochem Syst Ecol 38:935–957

    Article  CAS  Google Scholar 

  39. Gonçalves S, Romano A (2016) The medicinal potential of plants from the genus Plantago (Plantaginaceae). Ind Crops Prod 83:213–226

    Article  CAS  Google Scholar 

  40. Gonçalves S, Grevenstuk T, Martins N, Romano A (2015) Antioxidant activity and verbascoside content in extracts from two uninvestigated endemic Plantago spp. Ind Crops Prod 65:198–202

    Article  CAS  Google Scholar 

  41. IUPACIUB Commission in Biochemical Nomenclature (CBN) (1976) Nomenclature of cyclitols. Recommendations. Biochem J 153:23–31

    Article  Google Scholar 

  42. Bajko E, Kalinowska M, Borowski P, Siergiejczyk L, Lewandowski W (2016) 5-O-Caffeoylquinic acid: a spectroscopic study and biological screening for antimicrobial activity. LWT Food Sci Technol 65:471–479

    Article  CAS  Google Scholar 

  43. Mazzutti S, Riehl CAS, Ibañez E, Ferreira SRS (2017) Green-based methods to obtain bioactive extracts from Plantago major and Plantago lanceolata. J Supercrit Fluids 119:211–220

    Article  CAS  Google Scholar 

  44. Attri S, Singh N, Singh TR, Goel G (2017) Effect of in vitro gastric and pancreatic digestion on antioxidant potential of fruit juices. Food Biosci 17:1–6

    Article  CAS  Google Scholar 

  45. Jara-Palacios JM, Gonçalves S, Hernanz D, Heredia JF, Romano A (2018) Effects of in vitro gastrointestinal digestion on phenolic compounds and antioxidant activity of different white winemaking byproducts extracts. Food Res Int 109:433–439

    Article  CAS  Google Scholar 

  46. Martínez-Las Heras R, Pinazo A, Heredia A, Andrés A (2017) Evaluation studies of persimmon plant (Diospyros kaki) for physiological benefits and bioaccessibility of antioxidants by in vitro simulated gastrointestinal digestion. Food Chem 214:478–485

    Article  CAS  PubMed  Google Scholar 

  47. Siracusa L, Kulišić-Bilušić T, Politeo O, Krause I, Dejanović B, Ruberto G (2011) Phenolic composition and antioxidant activity of aqueous infusions from Capparis spinosa L. and Crithmum maritimum L. before and after submission to a two-step in vitro digestion model. J Agric Food Chem 59:12453–12459

    Article  CAS  PubMed  Google Scholar 

  48. Jayawardena N, Watawana MI, Waisundara VY (2015) Evaluation of the total antioxidant capacity, polyphenol contents and starch hydrolase inhibitory activity of ten edible plants in an in vitro model of digestion. Plant Foods Hum Nutr 70:71–76

    Article  CAS  PubMed  Google Scholar 

  49. Chen G-L, Chen S-G, Xie Y-Q, Chen F, Zhao Y-Y, Luo C-X, Gao Y-Q (2015) Total phenolic, flavonoid and antioxidant activity of 23 edible flowers subjected to in vitro digestion. J Funct Food 17:243–259

    Article  CAS  Google Scholar 

  50. Pavan V, Sancho RAS, Pastores GM (2014) The effect of in vitro digestion on the antioxidant activity of fruit extracts (Carica papaya, Artocarpus heterophillus and Annona marcgravii). LWT-Food Sci Technol 59:1247–1251

    Article  CAS  Google Scholar 

  51. Celep E, Charehsaz M, Akyüz S, Acar ET, Yesilada E (2015) Effect of in vitro gastrointestinal digestion on the bioavailability of phenolic components and the antioxidant potentials of some Turkish fruit wines. Food Res Int 78:209–215

    Article  CAS  PubMed  Google Scholar 

  52. Wootton-Beard PC, Moran A, Ryan L (2011) Stability of the total antioxidant capacity and total polyphenol content of 23 commercially available vegetable juices before and after in vitro digestion measured by FRAP, DPPH, ABTS and Folin–Ciocalteu methods. Food Res Int 44:217–224

    Article  CAS  Google Scholar 

  53. Henning SM, Zhang Y, Rontoyanni VG, Huang J, Lee RP, Trang A, Heber D (2014) Variability in the antioxidant activity of dietary supplements from pomegranate, milk thistle, green tea, grape seed, goji, and acai: effects of in vitro digestion. J Agric Food Chem 62:4313–4321

    Article  CAS  PubMed  Google Scholar 

  54. Wong Y, Tan C, Long K, Nyam K (2014) In vitro simulated digestion on the biostability of Hibiscus cannabinus L. seed extract. Czech J Food Sci 32:177–181

    Article  CAS  Google Scholar 

  55. Arenas EH, Trinidad TP (2017) Fate of polyphenols in pili (Canarium ovatum Engl.) pomace after in vitro simulated digestion. Asian Pac J Tropical Biomed 7:53–58

    Article  Google Scholar 

  56. Guldiken B, Toydemir G, Nur Memis K, Okur S, Boyacioglu D, Capanoglu E (2016) Home-processed red beetroot (Beta vulgaris L.) products: changes in antioxidant properties and bioaccessibility. Int J Mol Sci 17:1–13

    Article  CAS  Google Scholar 

  57. Jayawardena N, Watawana MI, Waisundara VI (2015) The total antioxidant capacity, total phenolics content and starch hydrolase inhibitory activity of fruit juices following pepsin (gastric) and pancreatin (duodenal) digestion. J Verbr Lebensm 10:349–357

    Article  CAS  Google Scholar 

  58. Alipieva K, Korkina L, Orhan IE, Georgiev MI (2014) Verbascoside—a review of its occurrence, (bio)synthesis and pharmacological significance. Biotechnol Adv 32:1065–1076

    Article  CAS  PubMed  Google Scholar 

  59. Zhou A, Sadik AO (2008) Comparative analysis of quercetin oxidation by electrochemical, enzymatic, autoxidation, and free radical generation techniques: a mechanistic study. J Agric Food Chem 56:12081–12091

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work received financial support from the European Union (FEDER funds through COMPETE). This work also received financial support from National Funds (FCT/MEC, Fundação para a Ciência e Tecnologia/Ministério da Educação e Ciência) through project UID/QUI/50006/2013, co-financed by European Union (FEDER under the Partnership Agreement PT2020), from Programa de Cooperación Interreg V-A España – Portugal (POCTEP) 2014–2020 (project 0377_IBERPHENOL_6_E) and from the project INTERREG - MD.Net: When Brand Meets People. S. Gonçalves acknowledges the financial support from FCT.

Author information

Authors and Affiliations

  1. Faculty of Sciences and Technology, MeditBio, University of Algarve, Campus de Gambelas, Ed. 8, 8005-139, Faro, Portugal

    Sandra Gonçalves, Elsa Moreira & Anabela Romano

  2. REQUIMTE/LAQV, Laboratório de Farmacognosia, Departamento de Química, Faculdade de Farmácia, Universidade do Porto, Rua de Jorge Viterbo Ferreira, n. 228, 4050-313, Porto, Portugal

    Paula B. Andrade & Patrícia Valentão

Authors
  1. Sandra Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elsa Moreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paula B. Andrade
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patrícia Valentão
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anabela Romano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anabela Romano.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Compliance with ethics requirements

This article does not contain any studies with human or animal subjects.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gonçalves, S., Moreira, E., Andrade, P.B. et al. Effect of in vitro gastrointestinal digestion on the total phenolic contents and antioxidant activity of wild Mediterranean edible plant extracts. Eur Food Res Technol 245, 753–762 (2019). https://doi.org/10.1007/s00217-018-3197-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00217-018-3197-y

Keywords

  • Beta maritima L.
  • Gastric digestion
  • Intestinal digestion
  • Plantago major L.
  • Oxalis pes-caprae L.
  • Scolymus hispanicus L