Agricultural Reviews

  • Chief EditorPradeep K. Sharma

  • Print ISSN 0253-1496

  • Online ISSN 0976-0741

  • NAAS Rating 4.84

Frequency :
Quarterly (March, June, September & December)
Indexing Services :
AGRICOLA, Google Scholar, CrossRef, CAB Abstracting Journals, Chemical Abstracts, Indian Science Abstracts, EBSCO Indexing Services, Index Copernicus
Submit

Reviewer Article

Agricultural Reviews, volume 43 issue 2 (june 2022) : 178-185

Betalains in Animal Nutrition and Health: Importance as Animal Feed Supplements- A Review

Belhadj Slimen Imen, Najar Taha, Pacheo Wilmer
1Department of Animal, Food and Halieutic Resources, National Agronomic Institute of Tunisia, 43 Av Charles Nicolle 1082 Tunis, Tunisia.
Cite article:- Imen Slimen Belhadj, Taha Najar, Wilmer Pacheo (2022). Betalains in Animal Nutrition and Health: Importance as Animal Feed Supplements- A Review. Agricultural Reviews. 43(2): 178-185. doi: 10.18805/ag.R-155.

ABSTRACT

In recent years, betalain-containing fruits and vegetables have gained increased importance in research and food industry. The extracted betalains are safe to consume and are considered as health promoting molecules. In vitro and in vivo studies highlighted the antioxidant and the biological activities of these pigments. However, the bioavailability of betalains, their ability to protect/treat oxidative stress related diseases and their health promoting properties were investigated using mainly rodents and human models. To enlarge the sphere of application of these pigments, research trials should be extended to farm animals. This paper details the bioavailabilty and the in vivo radical scavenging activity of these molecules and proposes their use as natural animal feed additives for future debate.

REFERENCES


  1. Aly, A.H., Debbab, A., Proksch, P. (2013). Fungal endophytes- Secret producers of bioactive plant metabolites. Pharmazie. 68: 499-505.

  2. Archile-Contreras, A.C., Purslow, P.P. (2011). Oxidative stress may affect meat quality by interfering with collagen turnover by muscle fibroblasts. Food Res. Intern. 44: 582-588.

  3. Atiba, E.M., Laban, R.K., Zewei, S., Kingzhang, Z., Aschalew, N.D. (2021). Implication of tannin containing plants for productivity and health in small ruminant animals: A review. Aric. Rev. 42: 156-165.

  4. Avanzo, J.L., De Mendoca, C.X., Piccoli, S.M., De Cerqueira, C. (2001). Effect of vitamin E and selenium on resistance to oxidative stress in chicken superficial pectoralis muscle. Comp. Biochem. Physiol. 129: 163-173.

  5. Bascom-Slack, C.A., Arnold, A.E., Strobel, S.A. (2012). IBI series winner. Student-directed discovery of the plant microbiome and its products. Sci. 338: 485-486.

  6. Belhadj Slimen, I., Chabaane, H., Chaar, H., Mabrouk, M., Najar, T., Ounallah, M.K., Abderrabba, M. (2020). Bioactive molecules and pigments in cladodes, fruits and peels of Tunisian Opuntia ficus-indica f. inermis. J. Anim. Plant. Sci. 45: 7944-7963.

  7. Belhadj Slimen, I., Najar, T., Abderrabba, M. (2021). Bioactive Compounds of Prickly Pear [Opuntia ficus-indica (L.) Mill]. In: Bioactive Compounds in Underutilized Vegetables and Legumes. [Murthy, H.N., Paek, K.Y. (eds.)], Reference Series in Phytochemistry, Springer Nature, Switzerland, AG. pp. 1-40.

  8. Belhadj Slimen, I., Najar, T., Ghram, A., Dabbebi, H., Ben Mrad, M., Abdrabbah, M. (2014). Reactive oxygen species, heat stress and oxidative-induced mitochondrial damage. A review. Int. J. Hyperth. 30: 513-523.

  9. Belhadj Slimen, I., Najar, T., Abdrrabba, M. (2017). Chemical and antioxidant properties of betalains. J. Agric. Food Chem. 65: 675-689.

  10. Belhadj Slimen, I., Chabaane, H., Chniter, M., Mabrouk, M., Ghram, A., Miled, K., Behi, I., Abdrrabba, M., Najar, T. (2019). Thermoprotective properties of Opuntia ficus-indica f. inermis cladodes and mesocarps on sheep lymphocytes. J.Therm. Biol. 81: 73-81.

  11. Belhadj Slimen, I., Najar, T., Ghram, A., Abdrrabba, M. (2016). Heat stress effects on livestock: Molecular, cellular and metabolic aspects: A review. J Anim Physiol Anim Nutr. 100: 401-412.

  12. Castillo, C., Hernandez, J., Bravo, A., Lopez-Alonso, M., Pereira, V., Benedito, J.L. (2005). Oxidative status during late pregnancy and early lactation in dairy cows. Vet J. 169: 286-292.

  13. Celi, P., (2010). The role of oxidative stress in small ruminants’ health and production. R. Bras. Zootec. 39: 348-363.

  14. Celi, P., Gabai, G. (2015). Oxidant/Antioxidant Balance in Animal Nutrition and Health: The Role of Protein Oxidation. Front Vet Sci. 2. DOI: 10.3389/fvets.2015.00048.

  15. Chiquette, J. (2009). Evaluation of the protective effect of probiotics fed to dairy cows during a subacute ruminal acidosis challenge. Anim. Feed Sci. Technol. 153: 278-291.

  16. Das, S.K. (2018). Impact of climate change (heat stress) on livestock: Adaptation and mitigation strategies for sustainable production. Agric. Rev. 39: 130-136.

  17. Demain, A.L., Fang, A. (2000). The natural functions of secondary metabolites. Adv Biochem. Eng. Biotechnol. 69: 1-39.

  18. EAEMP (The European Agency for the Evaluation of Medicinal Products). (2010). Note for guidance on the investigation of bioavailability and bioequivalence. 1-18.

  19. El Gamal, A.A., AlSaid, M.S., Raish, M., Al-Sohaibani, M., Al-Massarani, S.M., Ahmad, A., Hefnawy, M., Al-Yahya, M., Basoudan, O.A., Rafatullah, S. (2014). Beetroot (Beta vulgaris L.) extract ameliorates gentamicin-induced nephrotoxicity associated oxidative stress, inflammation and apoptosis in rodent model. Mediat. Inflamm. 983- 952.

  20. Esatbeyoglu, T., Wagner, A.E., Motafakkerazad, R., Nakajima, Y., Matsugo, S., Rimbach, G. (2014). Free radical scavenging and antioxidant activity of betanin: Electron spin resonance spectroscopy studies and studies in cultured cells. Food Chem. Toxicol. 73: 119-126.

  21. Francis, F.J. (1999). Anthocyanins and betalains. In: Colorants. [Francis, F.J. (eds.)], Eagan Press, St. Paul, MN. pp. 55- 66.

  22. Gabai, G., Testoni, S., Piccinini, R., Marinelli, L., Stradaioli, G. (2004). Oxidative stress in primiparous cows in relation to dietary starch and the progress of lactation. Anim. Sci. 79: 99-108.

  23. Garg, S. (2020). Flavonoids: Biosynthesis, metabolism, mechanism of antioxidation and clinical implications: A review. Agric. Rev. 41: 227-237.

  24. Gobert, M., Martin, B., Ferlay, A., Chilliard, Y., Graulet, B., Pradel, P., Bauchart, D., Duran, D. (2009). Plant polyphenols associated with vitamin E can reduce plasma lipoperoxidation in dairy cows given n-3 polyunsaturated fatty acids. J. Dairy Sci. 92: 6095-6104.

  25. Guevara, J.C., Suassuna, P., Felker, P. (2009). Opuntia forage production system: Status and prospects for rangeland application. Rangel. Ecol. Manag. 62: 428-434.

  26. Holt, R.R., Lazarus, S.A., Sullards, M.C., Zhu, Q.Y., Schramm, D.D., Hammrstone, J.F., Fraga, G.C., Schmitz, H.H., Keen, C. (2002). Procyanidin dimer B2 [epicathechin-(4beta-8)-epicathechin] in human plasma after the consumption of a flavonol-rich cocoa. Am J Clin Nutr. 76: 798-804.

  27. Hooper, P.L., Hooper, P.L., Tytell, M., Vígh, L. (2010). Xenohormesis: Health benefits from an eon of plant stress response evolution. Cell Stress Chaper. 15: 761-770.

  28. Hutton, P.G., Nagaraja, T.G., White, C.L., Vercoe, P.E. (2010). Screening plants for the antimicrobial control of lactic acidosis. In: Ruminant Livestock. [Vercoe, P.E., Makkar, H.P.S., Schlink, A.C., (eds.)], Springer, The Netherlands, 2010. pp. 159-189.

  29. Jackman, R.L., Smith, J.L. (1996). Anthocyanins and betalains. In: Natural Food Colorants. [Hendry, G.F., Houghton, J.D., eds.], Blackie Academic and Professional, London. pp. 244-309.

  30. Joachim, J.A., Joseph, O.A., Sunday, A.O. (2010). Effects of heat stress of some blood parameters and egg production of Shika Brown layer chickens transported by road. Biol. Res. 43: 183-189.

  31. Kanner, J., Harel, S. (2001). Granit, R. Betalains-A new class of dietary antioxidants. J. Agric. Food Chem. 49: 5178-5185.

  32. Karou, D., Savadogo, A., Canini, A., Yameogo, S., Montesano, C., Simpore, J., Colizzi, V., Traore, A. (2005). Antibacterial activity of alkaloids from Sida acuta. Afr. J. Biotechnol. 4: 1452-1457.

  33. Kayser, O., Kiderlen, A.F., Croft, S.L. (2003). Natural products as antiparasitic drugs. Prasitol. Res. 90: S55-S62.

  34. Khan, M.I. (2016). Plant betalains: Safety, antioxidant activity, clinical efficiency and bioavailability. Compr Rev. Food Sci. Food Saf. 15: 316-330.

  35. Krajka-Kuźniak, V., Paluszczak, J., Szaefer, H., Baer-Dubowska, W. (2013). Betanin, a beetroot component, induces nuclear factor erythroid-2-related factor 2-mediated expression of detoxifying/antioxidant enzymes in human liver cell lines. Br. J. Nutr. 110: 2138-2149.

  36. Krajka-Kuźniak, V., Szaefer, H., Ignatowicz, E., Adamska, T., Baer- Dubowska, W. (2012). Beetroot juice protects against N-nitrosodiethylamine-induced liver injury in rats. Food. Chem. Toxicol. 50: 2027-2033.

  37. Kujawska, M., Ignatowicz, E., Murias, M., Ewertowska, M., Miko³ajczyk, K., Jodynis-Liebert, J. (2009). Protective effect of red beetroot against carbon tetrachloride and N-nitrosodiethylamine-induced oxidative stress in rats. J. Agric. Food Chem. 57: 2570-2575.

  38. Kumar, A., Ahmad, F., Zaidi, S., (2019). Importance of bioactive compounds present in plant products and their extraction: A review. Agric. Rev. 40: 249-260.

  39. Le Bellec, F., Vaillant, F., Imbert, E., (2006). Pitahaya (Hylocereus spp.): A new fruit crop, a market with a future. Fruits. 61: 237-250.

  40. Lee, J.H., Son, C.W., Kim, M.Y., Kim, M.H., Kim, H.R., Kwak, E.S., Kim, S., Kim, M.R. (2009). Red beet (Beta vulgaris L.) leaf supplementation improves antioxidant status in C57BL/6J mice fed high fat high cholesterol diet. Nutr. Res. Pract. 3: 114-121.

  41. Lu, X., Wang, Y., Zhang, Z. (2009). Radioprotective activity of betalains from red beets in mice exposed to gamma irradiation. Eur. J. Pharmacol. 615: 223-227.

  42. Lykkesfeldt, J., Svendsen, O. (2007). Oxidants and antioxidants in disease: Oxidative stress in farm animals. Vet J. 173: 502-511.

  43. Martinez, R.M., Longhi-Balbinot, D.T., Zarpelon, A.C., Staurengo Ferrari, L., Baracat, M.M., Georgetti, S.R., Sassonia, R.C.,Verri Jr., W.A., Casagrande, R. (2015). Anti- inflammatory activity of betalain-rich dye of Beta vulgaris: Effect on edema, leukocyte recruitment, superoxide anion and cytokine production. Arch. Pharmacol Res. 38: 494- 504.

  44. Meissner, H.H., Henning, P.H., Horn, C.H., Leeuw, K.J., Hagg, F.M., Fouché, G. (2010). Ruminal acidosis: A review with detailed reference to the controlling agent Megasphaera elsdenii NCIMB 41125 S. Afr. J. Anim. Sci. 40: 79-100.

  45. Mickdam, E., Khiaosa-ard, R., Metzler-Zebeli, B.U., Klevenhusen, F., Chizzola, R., Zebeli, Q. (2016). Rumen microbial abundance and fermentation profile during severe subacute ruminal acidosis and its modulation by plant derived alkaloids in vitro. Anaerobe 39: 4-13.

  46. Moreira da Silva, F., Marques, A., Chaveiro A. (2010). Reactive oxygen species: A double-edged sword in reproduction. Open Vet. Sci. J. 4: 127-133.

  47. Morimoto, R.I., Tissieres, A., Georgopoulos, C. (1990). Stress proteins in biology and medicine. Cold Spring Harbor Laboratory Press, New York. 1990. 450p.

  48. Mousa, W.K., Raizada, M.N., (2013). The diversity of anti-microbial secondary metabolites produced by fungal endophytes: An interdisciplinary perspective. Front. Microbiol. 4 : 65.

  49. Neelwarne, B., Halagur, S.B. (2013). Red Beet: An Overview. In: Red Beet Biotechnology: Food and Pharmaceutical Application. [Neelwarne, B. (eds.)], Springer, Heidlberg Dordrecht, New York. 2013. pp. 1-44.

  50. Nguyen, T., Nioi, P., Pickett, C.B., (2009). The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J. Biol. Chem. 284: 13291-13295.

  51. Nisar, A.N., Sultana, M., Ashraf waiz, H., (2013). Oxidative stress- Threat to animal health and production. Int. J. Lives. Res. 76-83.

  52. Pavlov, A., Kovatcheva, P., Tuneva, D., Ilieva, M., Bley, T. (2005). Radical Scavenging activity and stability of betalains from Beta vulgaris hairy root culture in simulated conditions of human gastrointestinal tract. Plant Foods Human Nutr. 60: 4347.

  53. Pavokovic, D., Krsnik-Rasol, M. (2011). Complex biochemistry and biotechnological production of betalains. Food Technol. Biotechnol. 49: 145-155.

  54. Pedernera, M., Celi, P., García, S.C., Salvin, H.E., Barchia, I., Fulkerson, W.J. (2010). Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture. Vet J. 186: 352-357.

  55. Pietrzkowski, Z., Nemzer, B., Spórna, A., Stalica, P., Tresher, W., Keller, R., Jiminez, R., Michalowski, T., Wybraniec, S. (2010). Influence of betalin-rich extracts on reduction of discomfort associated with osteoarthritis. New. Med. 1: 12-17.

  56. Satoh, T., McKercher, S.R., Lipton, S.A. (2014). Reprint of: Nrf2/ ARE-mediated antioxidant actions of pro-electrophilic drugs. Free Radic. Biol. Med. 66: 45-57.

  57. Schroeter, H., Heiss, C., Balzer, J., Kleinbongrad, P., Keen, C.L., Hollenberg, N.K., Sies, H., Kwik-Uribe, C.L., Schmitz, H.H., Kelm, M. (2006). (-)-Epicathechin mediates beneficial effects of flavonolrich cocoa on vascular function in humans. Proc Nat Acad Sci USA. 103: 1024-1029.

  58. Shea, K. (2012). Importation of fresh pitaya from central America into the continental United States (7 CFR Part 319 No. FR Doc No: 2012-9066), Animal and plant health inspection service, USDA. Deparment of Agriculture, Washington 2012, DC.

  59. Shunmugadevi, C., Anbu Radhika, S. (2020). Bioactivity of plant extracts against cowpea bruchid Callosobruchus maculatus (Fab): A review. Agric. Rev. 41: 185-200.

  60. Siriwardhana, N., Shahidi, F., Jeon, Y.J. (2006). Potential antioxidative effects of cactus pear fruit (Opuntia ficus indica) extract on radical scavenging and DNA damage reduction in human peripheral lymphocytes. J. Food Lipids. 13: 445-458.

  61. Sordillo, L.M., Aitken, S.L. (2009). Impact of oxidative stress on the health and immune function of dairy cattle. Vet Immunol Immunopathol. 128: 104-109.

  62. Steglich, W., Strack, D., (1990). Betalains. In: The Alkaloids, Chemistry and Pharmacology. [Brossi, A. (eds.)], Academic Press, London, 1990. pp.1-62.

  63. Stintzing, F.C., Carle, R. (2004). Functional properties of anthocyanins and betalains in plants, food and in human nutrition. Trends Food Sci. Technol. 15: 19-38.

  64. Strobel, G., Daisy, B., Castillo, U., Harper, J. (2004). Natural products from endophytic microorganisms. J. Nat. Prod. 67: 257-268.

  65. Sun, H., Pang, K.S. (2008). Permeability, transport and metabolism of solutes in Caco-2 cell monolayers: A theoretical study. Drug Metab. Dispo. 36: 102-123.

  66. Szaefer, H., Krajka-Kuźniak, V., Ignatowicz, E., Adamska, T., Baer-Dubowska, W. (2014). Evaluation of the effect of beetroot juice on DMBA-induced damage in liver and mammary gland of female Sprague-Dawley rats. Phytother. Res. 28: 55-61.

  67. Tesoriere, L., Allegra, M., Butera, D., Livrea M.A. (2004a). Absorption, excretion and distribution of dietary antioxidant betalains in LDLs: Potential health effects of betalains in humans. Am. J. Clin. Nutr. 80: 941-945.

  68. Tesoriere, L., Attanzio, A., Allegra, M., Gentile, C., Livrea, M.A. (2014). Indicaxanthin inhibits NADPH oxidase (NOX)-1 activation and NF-kB-dependent release of inflammatory mediators and prevents the increase of epithelial permeability in IL-1b-exposed Caco-2 cells. Br. J. Nutr. 111: 415-423.

  69. Tesoriere, L., Butera, D., D’Arpa, D. (2003). Increased resistance to oxidation of betalain-enriched human low density lipoproteins. Free Radic. Res. 37: 689-696.

  70. Tesoriere, L., Butera, D., Pintaudi, A.M., Allegra, M., Livrea, M.A. (2004b). Supplementation with cactus pear (Opuntia ficus indica) fruit decreases oxidative stress in healthy humans: a comparative study with vitamin C. Am. J. Clin. Nutr. 80: 391-395.

  71. Tesoriere, L., Farrari, M., Angileri, F., Gentile, C., Livera, M.A. (2008). In vitro Digestion of Betalainic Foods. Stability and Bioaccessibility of Betaxanthins and Betacyanins and Antioxidative Potential of Food Digesta. J. Agric. Food Chem. 56: 10487-10492.

  72. Tesoriere, L., Butera, D., Allegra, M., Fazzari, M., Livrea, M.A. (2005). Distribution of betalain pigments in red blood cells after consumption of cactus pear fruits and increased resistance of the cells to ex vivo induced oxidative hemolysis in humans. J. Agric. Food Chem. 23: 1266- 1270.

  73. Toutain, P.L., Bousquet-Melou, A. (2004). Bioavailability and its assessment. J. Vet. Pharmacol. Ther. 27: 455-66.

  74. Tschirner, K. (2004). Untersuchungen zur Wirksamkeit und zum Nachweis des pflanzlichen Alkaloids Sanguinarin beim Schwein. PhD Thesis, der Christian-Albert-Universität zu Kiel, Germany, 2004. p. 110.

  75. Turco-Liveri, M.L., Sciascia, L., Allegra, M., Tesoriere, L., Livrea, M.A. (2009). Partition of indicaxanthin in membrane biomimetic systems. A kinetic and modeling approach. J. Agric. Food Chem. 57: 10959-10963.

  76. Turco-Liveri, M.L., Sciascia, L., Lombardo, R., Tesoriere, L., Passante, E., Livrea, M.A. (2007). Spectrophotometric evidence for the solubilization site of betalain pigments in membrane biomimetic systems. J. Agric. Food Chem. 55: 2836-2840.

  77. Turrens, J.F. (2003). Mitochondrial formation of reactive oxygen species. J. Physiol. 555: 335-344.

  78. Vaillant, F., Perez, A., Davila, I., Dornier, M., Reynes, M. (2005). Colorant and antioxidant properties of red-purple pitahaya (Hylocereus sp.). Fruits. 60: 3-12.

  79. Verma, V.C., Kharwar, R.N., Strobel, G.A. (2009). Chemical and functional diversity of natural products from plant associated endophytic fungi. Nat. Prod. Commun. 4: 1511-1532.

  80. Vidal, P.J., López-Nicolás, J.M., Gandía-Herrero, F., García- Carmona, F. (2014). Inactivation of lipoxygenase and cyclooxygenase by natural betalains and semi-synthetic analogues. Food Chem. 154: 246-254.

  81. Vieira, S.L., Oyarzabal, O.A., Freitas, D.M., Berres, J., Peña, J.E.M., Torres, C.A., Coneglian, J.L.B. (2008). Performance of broilers fed diets supplemented with sanguinarine-like alkaloids and organic acids. J. Appl. Poult. Res. 17: 128- 133.

  82. Villalba, J.J., Provenza, F.D. (2007). Self-medication and homeostatic behavior in herbivors: learning about the benefits of nature’s pharmacy. Animal. 1: 1360-1370.

  83. Vulić, J.J., Ćebović, T.N., Čanadanović-Brunet, J.M., Ćetković, G.S., Čanadanović, V.M., Djilas, S.M., Tumbas Šaponjac, V.T. (2014). In vivo and in vitro antioxidant effects of beetroot pomace extracts. J. Funct. Foods. 6: 168-175.

  84. Waller, P.J. (2006). Sustainable nematode parasite control strategies for ruminant livestock by grazing management and biological control. Anim. Feed Sci. Technol. 126: 277- 289.

  85. Yang, W.Z., Ametaj, B.N., Benchaar, C., He, M.L., Beauchemin, K.A. (2010). Cinnamaldehyde in feedlot cattle diets: Intake, growth performance, carcass characteristics and blood metabolites. J. Anim. Sci. 88: 1082-1092.

  86. Yu, H., Zhang, L., Li, L., Zheng, C., Guo, L., Li, W., Sun, P., Qin, L. (2010). Recent developments and future prospects of antimicrobial metabolites produced by endophytes. Microbiol. Res. 165: 437-449.

  87. Zielińska-Przyjemska, M., Olejnik, A., Kostrzewa, A., Łuczak, M., Jagodziński, P.P., Baer-Dubowska, W. (2012). The beetroot Component betanin modulates ROS production, DNA damage and apoptosis in human polymorphonuclear neutrophils. Phytother. Res. 26: 845-852.
Reviewed By

Download Article
In this Article
    Contact us
    Follow us

    Editorial Board

    View all (0)