Environmentally friendly achiote seed extracts with higher δ-tocotrienol content have higher in vitro and in vivo antioxidant activity than the conventional extract

Abstract

Achiote (Bixa orellana) is highly appreciated as a condiment and as the main source of bixin and tocotrienols, both having antioxidant properties. To explore the possibility of maximizing the antioxidant activity of achiote seed extracts using clean methodologies, the use of sonication and green solvents were tested. Ethyl lactate, isopropyl acetate, and ethanol combined with probe sonication produced the best results, obtaining similar bixin contents but higher δ-tocotrienol contents, as well as significantly higher in vitro and in vivo antioxidant activity compared with the maceration method extract, requiring low energy and saving time and solvents. The probe-sonicated achiote extract with the highest δ-tocotrienol content was better at increasing the Caenorhabditis elegans resistance to oxidative stress than the extract obtained through maceration. This is the first report about the effect of sonication combined with green solvents on the bixin and δ-tocotrienol content in achiote seed extracts and its relevance on the in vitro and in vivo antioxidant activity.

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References

  1. Aan G, Zainudin M, Karim N, Wan W (2013) Effect of tocotrienol-rich fraction on the lifespan and oxidative biomarkers in Caenorhabditis elegans under oxidative stress. Clinics (Sao Paulo) 68:599–604. https://doi.org/10.6061/clinics/2013(05)04

    Article  Google Scholar 

  2. Adachi H, Ishii N (2000) Effects of tocotrienols on life span and protein carbonylation in Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 55:B280–B285

    CAS  Article  Google Scholar 

  3. Aggarwal B, Sundaram C, Prasad S, Kannappan R (2010) Tocotrienols, the vitamin E of the 21st century: its potential against cancer and other chronic diseases. Biochem Pharmacol 80:1613–1631. https://doi.org/10.1016/j.bcp.2010.07.043

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Alavez S, Vantipalli M, Zucker D, Klang I, Lithgow G (2011) Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan. Nature 472:226–229. https://doi.org/10.1038/nature09873

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. American Chemical Society (2007) Introduction: green chemistry. Chem Rev 107:2167–2168. https://doi.org/10.1021/cr0783784

    CAS  Article  Google Scholar 

  6. Balaswamy K, Prabhakara-Rao PG, Satyanarayana A, Rao DG (2006) Stability of bixin in annatto oleoresin and dye powder during storage. J Food Sci Technol 39:952–956. https://doi.org/10.1016/j.lwt.2005.07.004

    CAS  Article  Google Scholar 

  7. Byrne FP, Jin S, Paggiola G, Petchey THM, Clark JH, Farmer TJ, Hut AJ, McElroy CR, Sherwood J (2016) Tools and techniques for solvent selection: green solvent selection guides. Sustain Chem Process 4:7. https://doi.org/10.1186/s40508-016-0051-z

    CAS  Article  Google Scholar 

  8. Capello C, Fischer U, Hungerbüler K (2007) What is a green solvent? A comprehensive framework for the environmental assessment of solvents. Green Chem 9:927–934. https://doi.org/10.1039/b617536h

    CAS  Article  Google Scholar 

  9. Cardarelli C, Benassi MT, Mercadante A (2008) Characterization of different annatto extracts based on antioxidant and color properties. Food Sci Technol 41:1689–1693. https://doi.org/10.1016/j.lwt.2007.10.013

    CAS  Article  Google Scholar 

  10. Chisté RC, Benassi M, Mercadante AZ (2011) Effect of solvent type on the extractability of bioactive compounds, antioxidant capacity and colour properties of natural annatto extracts. Int J Food Sci Technol 46:1863–1870. https://doi.org/10.1111/j.1365-2621.2011.02693.x

    CAS  Article  Google Scholar 

  11. Dequigiovani G, Ferreyra-Ramos S, Alves-Pereira A, Gomes-Fabri E, Nogueira-Carvahlo P, Gomes da Silva M, Nogueira-Abdo M, Mello-Martins A, Clement C, Veasey E (2017) Genetic diversity and structure in a major Brazilian annatto (Bixa orellana) germplasm bank revealed by microsatellites and phytochemical compounds. Genet Resour Crop Evol 64:1775–1788. https://doi.org/10.1007/s10722-017-0535-z

    CAS  Article  Google Scholar 

  12. EU Regulatory Commission, No. 231/2012; Food Additives

  13. Falowo AB, Fayemi PO, Muchenje V (2014) Natural antioxidants against lipid-protein oxidative deterioration in meat and meat products: a review. Food Res Int 64:171–181. https://doi.org/10.1016/j.foodres.2014.06.022

    CAS  Article  PubMed  Google Scholar 

  14. FDA; 2017, CFR, Title 21, Chapter 1, Subchapter B, Apart 172: food additives permitted for direct addition to food for human consumptioN, Sub-apart F

  15. Fraser P, Pinto E, Holloway D, Bramley P (2000) Application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J 24:551–558. https://doi.org/10.1111/j.1365-313X.2000.00896.x

    CAS  Article  PubMed  Google Scholar 

  16. Frega N, Mozzon M, Bocci F (1998) Identification and estimation of tocotrienols in annatto lipid fraction by gas chromatography-mass spectrometry. J Am Oil Chem Soc 72:1723–1727. https://doi.org/10.1007/s11746-998-0323-1

    Article  Google Scholar 

  17. Giridhar P, Venugopalan A, Parimalan R (2014) A review on Annatto dye extraction, analysis and processing: a food technology perspective. J Sci Res Rep 3:327–348. https://doi.org/10.9734/JSRR/2014/5870

    Article  Google Scholar 

  18. Hussaana A, Suparmi Murti H (2018) Protective effect of bixin isolated from Bixa orellana L. seeds on UVB-induced inflammation and immunosuppression of the skin. Bangladesh J Med Sci 18:107–111. https://doi.org/10.3329/bjms.v18i1.39559

    Article  Google Scholar 

  19. Ito Y, Ishizuki K, Sekiguchi W, Tada A, Akiyama T, Sato K, Yamazaki T, Akiyama H (2012) Analysis of residual solvents in annatto extracts using static headspace gas chromatography method. Am J Analyt Chem 3:638–645. https://doi.org/10.4236/ajac.2012.39083

    CAS  Article  Google Scholar 

  20. Kotíková Z, Lachman J, Hejtmánková A, Hejtmánková K (2011) Determination of antioxidant activity and antioxidant content in tomato varieties and evaluation of mutual interactions between antioxidants. Food Sci Technol 44:1703–1710. https://doi.org/10.1016/j.lwt.2011.03.015

    CAS  Article  Google Scholar 

  21. Lucanic M, Lithgow G, Alavez S (2013) Pharmacological lifespan extension of invertebrates. Ageing Res Rev 12:445–458. https://doi.org/10.1016/j.arr.2012.06.006

    CAS  Article  PubMed  Google Scholar 

  22. Mène-Saffrané L, Jones D, DellaPenna D (2010) Plastochromanol-8 and tocopherols are essential lipid-soluble antioxidants during seed desiccation and quiescence in Arabidopsis. Proc Natl Acad Sci USA 107:17815–17820. https://doi.org/10.1073/pnas.1006971107

    Article  PubMed  Google Scholar 

  23. Oroian M, Escriche I (2015) Antioxidants: characterization, natural sources, extraction and analysis. Food Res Int 74:10–36. https://doi.org/10.1016/j.foodres.2015.04.018

    CAS  Article  PubMed  Google Scholar 

  24. Park JS, Mathison BD, Zawlocki BM, Chew BP (2016) Bixin uptake and antioxidative effect and role in immunoregulation in domestic cats. J Anim Sci 94:125–134. https://doi.org/10.2527/jas2015-9478

    CAS  Article  PubMed  Google Scholar 

  25. Quiroz JQ, Torres AC, Ramirez LM, Garcia MS, Gomez GC, Rojas J (2019) Optimization of the microwave-assisted extraction process of bioactive compounds from annatto seeds (Bixa orellana L.). Antioxidants (Basel) 8:37. https://doi.org/10.3390/antiox8020037

    CAS  Article  Google Scholar 

  26. Raddatz-Mota D, Pérez-Flores L, Carrari F, Insani M, Asis R, Mendoza-Espinoza A, Díaz de León-Sánchez F, Rivera-Cabrera F (2016) Chemical characterization and quantification of the pigment extraction yield of seven mexican accessions of Bixa orellana. Rev Mex Ing Quim 15:727–740

    CAS  Google Scholar 

  27. Rahmalia W, Fabre JF, Mouloungui Z (2015) Effects of cyclohexane/acetone ratio on bixin extraction yield by accelerated solvent extraction method. Proc Chem 14:455–464. https://doi.org/10.1016/j.proche.2015.03.061

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  29. Rojo de la Vega M, Krajisnik A, Zhang DD, Wondrak GT (2017) Targeting NRF2 for improved skin barrier function and photoprotection: focus on the achiote-derived apocarotenoid bixin. Nutrients 9:1371. https://doi.org/10.3390/nu9121371

    CAS  Article  PubMed Central  Google Scholar 

  30. Ruiz-Montañez G, Ragazzo-Sánchez J, Calderón-Santoyo M, Velázquez-de la Cruz G, de León J, Navarro-Ocaña A (2014) Evaluation of extraction methods for preparative scale obtention of mangiferin and lupeol from mango peels (Mangifera indica L.). Food Chem 159:267–272. https://doi.org/10.1016/j.foodchem.2014.03.009

    CAS  Article  PubMed  Google Scholar 

  31. Sen C, Khanna S, Roy S (2006) Tocotrienols: vitamin E beyond tocopherols. Life Sci 78:2088–2098

    CAS  Article  Google Scholar 

  32. Shahid-ul-Islam S, Rather L, Mahammad F (2016) Phytochemistry, biological activities and potential of annatto in natural colorant production for industrial applications: a review. J Adv Res 7:499–514. https://doi.org/10.1016/j.jare.2015.11.002

    CAS  Article  PubMed  Google Scholar 

  33. Sivakumar V, Vijaeeswarri J, Lakshim-Anna J (2011) Effective natural dye extraction from different plant materials using ultrasound. Ind Crops Prod 33:116–122. https://doi.org/10.1016/j.indcrop.2010.09.007

    CAS  Article  Google Scholar 

  34. Smith J (2006). Annatto extracts. Chemical and Technical Assessment. JECFA. 1-21

  35. Taham T, Olivera-Silva D, Barrozo MAS (2016) Improvement of bixin extraction from annatto seeds using a screen-topped spouted bed. Sep Purif Technol 158:313–321. https://doi.org/10.1016/j.seppur.2015.12.037

    CAS  Article  Google Scholar 

  36. Vilkhu K, Mawson R, Simons L, Bates D (2008) Applications and opportunities for ultrasound assisted extraction in the food industry: a review. Innov Food Sci Emerg Technol 9:161–169. https://doi.org/10.1016/j.ifset.2007.04.014

    CAS  Article  Google Scholar 

  37. Villa-Hernández J, Mendoza-Cardoso G, Mendoza-Espinoza J, Vela-Hinojosa C, Díaz de León-Sánchez F, Rivera-Cabrera F, Alia-Tejacal I, Pérez-Flores LJ (2017) Antioxidant capacity in vitro and in vivo of various ecotypes of Mexican plum (Spondias purpurea L.). J Food Sci 82:2576–2582. https://doi.org/10.1111/1750-3841.13862

    CAS  Article  PubMed  Google Scholar 

  38. Xu Z, Kong XQ (2017) Bixin ameliorates high fat diet-induced cardiac injury in mice through inflammation and oxidative stress suppression. Biomed Pharmacother 89:991–1004. https://doi.org/10.1016/j.biopha.2017.02.052

    CAS  Article  PubMed  Google Scholar 

  39. Zanifi A, Corbini G, La Rosa C, Dreassi E (2010) Antioxidant activity of tomato lipophilic extracts and interactions between carotenoids and α-tocopherol in synthetic mixtures. Food Sci Technol 43:67–72. https://doi.org/10.1016/j.lwt.2009.06.011

    CAS  Article  Google Scholar 

  40. Zhang H, Yang X, Zhao L, Wang Y (2009) Ultrasonic-assisted extraction of epimedin C fresh leaves of Epimedium and extraction mechanism. Innov Food Sci Emerg Technol 10:54–60. https://doi.org/10.1016/j.ifset.2008.09.007

    CAS  Article  Google Scholar 

  41. Zuorro A, Fidaleo M, Lavecchia R (2011) Enzyme-assisted extraction of lycopene from tomato processing waste. Enzyme Microb Technol 49:567–573. https://doi.org/10.1016/j.enzmictec.2011.04.020

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

We appreciate the kind disposition and collaboration of Alma Elizabeth Cruz Ph.D. for her technical support in this work. This research was supported by UAM and PRODEP-SEP Pre and Postharvest Science and Technology Network Program. SA is supported for a CONACyT Grant (288574). DRGL holds a CONACYT scholarship [300612] as part of his PhD studies (UAM Biotechnology Program PNPC-001466).

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Correspondence to Laura J. Pérez-Flores.

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Gómez-Linton, D.R., Navarro-Ocaña, A., Román-Guerrero, A. et al. Environmentally friendly achiote seed extracts with higher δ-tocotrienol content have higher in vitro and in vivo antioxidant activity than the conventional extract. J Food Sci Technol (2020). https://doi.org/10.1007/s13197-020-04764-0

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Keywords

  • Bixa orellana
  • Green solvents
  • Sonication
  • δ-Tocotrienol
  • Bioactive compounds
  • C. elegans