Antioxidant effectiveness of organically and non-organically grown red oranges in cell culture systems

Summary

Background

Consumers consider plant food products from organic origin healthier than the corresponding conventional plant foods. Clear experimental evidence supporting this assumption is still lacking.

Aim of the study

To determine if the organic red oranges have a higher phyto–chemical content (i. e., phenolics, anthocyanins and ascorbic acid), total antioxidant activity and in vitro bioactivity, in terms of protective effect against oxidative damage at cellular level, than nonorganic red oranges.

Methods

Total phenolics were measured using the Folin Ciocalteau assay, while total anthocyanins and ascorbic acid levels were determined by spectrophotometric and HPLC analysis, respectively. In addition, the total antioxidant activity of red orange extracts was measured by the ABTS•+ test. The ability of red orange extracts to counteract conjugated diene containing lipids and free radical production in cultured rat cardiomyocytes and differentiated Caco–2 cells, respectively, was assessed.

Results

Organic oranges had significantly higher total phenolics, total anthocyanins and ascorbic acid levels than the corresponding non–organic oranges (all p < 0.05). Moreover, the organic orange extracts had a higher total antioxidant activity than non–organic orange extracts (p < 0.05). In addition, our results indicate that red oranges have a strong capacity of inhibiting the production of conjugated diene containing lipids and free radicals in rat cardiomyocytes and differentiated Caco–2 cells, respectively. Statistically higher levels of antioxidant activity in both cell models were found in organically grown oranges as compared to those produced by integrated agriculture practice.

Conclusions

Our results clearly show that organic red oranges have a higher phytochemical content (i. e., phenolics, anthocyanins and ascorbic acid), total antioxidant activity and bioactivity than integrated red oranges. Further studies are needed to confirm whether the organic agriculture practice is likely to increase the antioxidant activity of other varieties of fruits and vegetables.

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References

  1. 1.

    Greene CUS (2000) Organic agriculture gaining ground. Agric Outlook 270:9–14

    Google Scholar 

  2. 2.

    Hamm U, Michelsen J (2000) In: Adolfi T, Lockeretz W, Niggli U (eds) IFOAM 2000 – The world Groes Organic. Proc. 13th Int. IFOAM Scientific Conf. IOS, Zurich, pp 507–510

  3. 3.

    Amiot MJ, Tacchini M, Aubert SY, Oleszek W (1995) Influence of cultivar, maturity stage and storage conditions on phenolic composition and enzymatic browning of pear fruits. J Agric Food Chem 43:1132–1137

    Article  CAS  Google Scholar 

  4. 4.

    Daniel O, Meier MS, Schlatter J, Frischknecht P (1999) Selected phenolic compounds in cultivated plants: ecologic functions, health implications, and modulation by pesticides. Environ Health Perspect 107:109–114

    CAS  Google Scholar 

  5. 5.

    Brandt K, Mølgaard JP (2001) Organic agriculture: does it enhance or reduce the nutritional value of plant foods? J Sci Food Agric 81:924–931

    Article  CAS  Google Scholar 

  6. 6.

    Sansavini S (1997) Integrated fruit production in Europe: Research and strategies for a sustainable industry. Sci Hort 68:25–36

    Google Scholar 

  7. 7.

    Castelluccio C, Pagana G, Melikian N, Bolwell GP, Pridham J, Sampson J, Rice– Evans C (1995) Antioxidant potential of intermediates in phenylpropanoid metabolism in higher plants. FEBS Lett 368:188–192

    Article  CAS  Google Scholar 

  8. 8.

    Rice–Evans CA, Miller NJ, Pagana G (1996) Structure–antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 20:933–956

    CAS  Google Scholar 

  9. 9.

    Maccarone E, Maccarone A, Rapisarda P (1985) Acylated anthocyanins from oranges. Ann Chim 75:79–86

    CAS  Google Scholar 

  10. 10.

    Maccarone E, Rapisarda P, Fanella F, Arena E, Mondello L (1998) Cyanidin– 3–(6”–malonyl)–beta–glucoside. One of the major anthocyanins in blood orange juice. It J Food Sci 10:367–372

    CAS  Google Scholar 

  11. 11.

    Rapisarda P, Tomaino A, Lo Cascio R, Bonina F, De Pasquale A, Saija A (1999) Antioxidant effectiveness as influenced by phenolic content of fresh orange juices. J Agric Food Chem 47:4718–4723

    Article  CAS  Google Scholar 

  12. 12.

    Duthie GG, Duthie SJ, Kyle JAM (2000) Plant polyphenols in cancer and heart disease: implications as nutritional antioxidants. Nutr Res Rev 13:79–106

    Article  CAS  Google Scholar 

  13. 13.

    Mouly PP, Gaydou EM, Faure R, Estienne JM (1997) Blood orange juice authentication using cinnamic acid derivatives. Variety differentiations associated with flavanone glucoside content. J Agric Food Chem 45:373–377

    Article  CAS  Google Scholar 

  14. 14.

    Rapisarda P, Crollo G, Fallico B, Tomaselli F, Maccarone E (1998) Hydroxycinnamic Acids as Markers of Italian Blood Orange Juices. J Agric Food Chem 46:464–470

    Article  CAS  Google Scholar 

  15. 15.

    Bordoni A, Hrelia S, Angeloni C, Giordano E, Guarnieri C, Caldarera CM, Biagi PL (2002) Green tea protection of hypoxia/reoxygenation injury in cultured cardiac cells. J Nutr Biochem 13:103–111

    CAS  Google Scholar 

  16. 16.

    Hidalgo IJ, Raub TJ, Borchardt RT (1989) Characterization of the human colon carcinoma cell line (Caco–2) as a model system for intestinal epithelial permeability. Gastroenterology 96:736–749

    CAS  Google Scholar 

  17. 17.

    Manna C, D'Angelo S, Migliardi V, Loffredi E, Mazzoni O, Morrica P, Galletti P, Zappia V (2002) Protective effect of the phenolic fraction from virgin olive oils against oxidative stress in human cells. J Agric Food Chem 50:6521–6526

    Article  CAS  Google Scholar 

  18. 18.

    Tarozzi A, Marchesi A, Cantelli–Forti G, Hrelia P (2004) Cold–storage affects antioxidant properties of apples in Caco–2 cells. J Nutr 134:1105–1109

    CAS  Google Scholar 

  19. 19.

    Sun J, Chu YF, Wu X, Liu RH (2002) Antioxidant and antiproliferative activities of common fruits. J Agric Food Chem 50:7449–7454

    CAS  Google Scholar 

  20. 20.

    Singleton VL, Orthofer R, Lamuela– Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin– Ciocalteu reagent. Methods Enzymol 299:152–178

    CAS  Google Scholar 

  21. 21.

    Asami DK, Hong YJ, Barrett DM, Mitchell AE (2003) Comparison of the total phenolic and ascorbic acid content of freeze–dried and air–dried marionberry, strawberry and corn grown using conventional, organic and sustainable agricultural practices. J Agric Food Chem 51:1237–1241

    Article  CAS  Google Scholar 

  22. 22.

    Lee HS, Chen CS (1998) Rates of Vitamin C loss and discoloration in clear orange juice concentrate during storage at temperature of 4–24 °C. J Agric Food Chem 46:4723–4727

    CAS  Google Scholar 

  23. 23.

    Rapisarda P, Fanella F, Maccarone E (2000) Reliability of analytical methods for determining anthocyanins in blood orange juices. J Agric Food Chem 48:2249–2252

    Article  CAS  Google Scholar 

  24. 24.

    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  Google Scholar 

  25. 25.

    Nagy A, Valen G, Ek B, Sellei PR, Sjöquist PO, Vaage J (1998) Effects of a novel, low–molecular weight inhibitor of lipid peroxidation on ischemia/ reperfusion injury in isolated rat hearts and in cultured cardiomyocytes. Free Radic Biol Med 24:1462–1469

    Article  CAS  Google Scholar 

  26. 26.

    Burton KP, McCord JM, Ghay G (1984) Myocardial alterations due to free radical generation. Am J Physiol 246:H776–H783

    CAS  Google Scholar 

  27. 27.

    Wang H, Joseph JA (1999) Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic Biol Med 27:612–616

    CAS  Google Scholar 

  28. 28.

    Baker SS, Baker RD Jr (1993) Caco–2 cell metabolism of oxygen–derived radicals. Dig Dis Sci 38:2273–2280

    Article  CAS  Google Scholar 

  29. 29.

    Carbonaro M, Mattera M, Nicoli S, Bergamo P, Cappelloni M (2002) Modulation of antioxidant compounds in organic vs. conventional fruit (Peach, Prunus persica L, and Pear, Pyrus communis L.). J Agric Food Chem 50: 5458–5462

    Article  CAS  Google Scholar 

  30. 30.

    Lattanzio V, DeCicco V, Di Venere D, Lima G, Salerno M (1994) Antifungal activity of phenolics against fungi commonly encountered during storage. It J Food Sci 1:23–30

    Google Scholar 

  31. 31.

    Woese K, Lange D, Boess C, Bogl KW (1997) A comparison of organically and conventionally grown foods – results of a review of the relevant literature. J Sci Food Agric 74:281–293

    Article  CAS  Google Scholar 

  32. 32.

    USDA Nutrient Database for Standard Reference, release 14 (2001) Nutrient Data Laboratory, Agricultural Research Service, Beltsville Human Nutrition Research Center: Beltsville, MD

  33. 33.

    Rapisarda P, Bellomo SE, Intrigliolo F (1992) Anthocyanin level in Italian blood oranges. Proc Int Soc Citric 3:1130–1133

    Google Scholar 

  34. 34.

    Mondello L, Cotroneo A, Errante G, Dugo G, Dugo P (2000) Determination of anthocyanins in blood orange juices by HPLC analysis. J Pharm Biomed Anal 23:191–195

    Article  CAS  Google Scholar 

  35. 35.

    Wang H, Cao G, Prior R (1996) Total antioxidant capacity of fruits. J Agric Food Chem 44:701–705

    CAS  Google Scholar 

  36. 36.

    Rice–Evans C, Miller NJ (1994) Total antioxidant status in plasma and body fluids. Methods Enzymol 234:279–293

    CAS  Google Scholar 

  37. 37.

    Trewavas A (2001) Urban myths of organic farming. Nature 410:409–410

    Article  CAS  Google Scholar 

  38. 38.

    Fisher BE (1999) Organic: What's in a name? Environ Health Perspect 107: A150–A153

    CAS  Google Scholar 

  39. 39.

    Schmidt CW (1999) An all–consuming issue. Environ Health Perspect 107:A144–A149

    CAS  Google Scholar 

  40. 40.

    Caris–Veyrat C, Amiot MJ, Tyssandier V, Grasselly D, Buret M, Mikolajczak M, Guilland JC, Bouteloup–Demange C, Borel P (2004) Influence of organic versus conventional agricultural practice on the antioxidant microconstituent content of tomatoes and derived purees; consequences on antioxidant plasma status in humans. J Agric Food Chem 52:6503–6509

    CAS  Google Scholar 

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Tarozzi, A., Hrelia, S., Angeloni, C. et al. Antioxidant effectiveness of organically and non-organically grown red oranges in cell culture systems. Eur J Nutr 45, 152–158 (2006). https://doi.org/10.1007/s00394-005-0575-6

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Key words

  • red orange
  • integrated agriculture
  • organic agriculture
  • phenolics
  • antioxidant activity