Evaluation of date palm pollen (Phoenix dactylifera L.) encapsulation, impact on the nutritional and functional properties of fortified yoghurt

Autoři: Wedad Mohamed El-Kholy aff001;  Tarek Nour Soliman aff002;  Amira Muhammad Galal Darwish aff003
Působiště autorů: Department of Dairy Research, Food Technology Research Institute (A.R.C.), Alexandria, Egypt aff001;  Department of Dairy, Food industries and nutrition Research Division, National Research Centre, Dokki, Cairo, Egypt aff002;  Department of Food Technology, Arid Lands Cultivation Research Institute (ALCRI), City of Scientific Research and Technological Applications (SRTA-City), New Borg El-Arab, Alexandria, Egypt aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222789


The aim of this study was to evaluate Egyptian date palm pollen (DPP) grains composition, physical and functional potentials in comparing with two forms; 80% ethanol extract, and nanoencapsulated form. Functional yoghurt fortified with DPP in three forms was prepared and their physicochemical, microstructure, texture and sensory characteristics were assessed. The micro morphology was explored via Scanning Electron Microscope (SEM). Fourier Transform Infrared (FTIR) spectroscopy was employed for functional groups detection. Phenolic compounds were detected by High Performance Liquid Chromatography (HPLC) while fatty acids were identified via Gas Liquid Chromatography (GLC). Cytotoxicity of DPP nanocapsules was evaluated against RPE1 cell line (BJ1). The Egyptian date palm pollen grains evaluation revealed its rich content of protein and carbohydrate (36.28 and 17.14 g/ 100g), high content of Fe, Zn and Mg (226.5, 124.4 and 318 mg/100g), unsaturated fatty acids ω-3, ω-6 and ω-9 (8.76, 20.26 and 7.11 g/100g, which was increased by ethanol extraction) and phenolic compounds especially catechin (191.73 μg/mL) which was pronounced in DPP antioxidant potentials (IC50 35.54 mg/g). The FTIR analyses indicated the presence of soluble amides (proteins) and polysaccharides (fibers) functional groups in DPP. Fortification with nanoencapsulated DPP proved to be safe and the recommended form due to the announced positive characteristics. Yoghurt fortification with DPP forms enhanced viscosity, syneresis and Water Holding Capacity (WHC), which can be considered a symbiotic functional product as it contained both probiotics (106 CFU/g) and prebiotics represented in DPP forms.

Klíčová slova:

Antioxidants – Ethanol – Fatty acids – Microstructure – Phenols – Pollen – Fourier transform infrared spectroscopy – Lecithin


1. McKinley MC. The nutrition and health benefits of yoghurt. Int J Dairy Technol. 2005;58(1):1–12. https://doi.org/10.1111/j.1471-0307.2005.00180.x

2. Lee WJ, Lucey JA. Formation and physical properties of yogurt. Asian-Australasian J Anim Sci. 2010;23(9):1127–36. https://doi.org/10.5713/ajas.2010.r.05

3. Mehmood ST, Masud T, Mahmood T, Masqsud S. Effect of Different Additives from local source on the quality of yoghurt. Pakistan J Nutr. 2008;7(5):695–9. doi: 10.3923/pjn.2008.695.699

4. Kroyer G, Hegedus N. Evaluation of bioactive properties of pollen extracts as functional dietary food supplement. Innov Food Sci Emerg Technol. 2001;2(3):171–4. https://doi.org/10.1016/S1466-8564(01)00039-X

5. Bishr M, Desoukey SY. Comparative Study of the Nutritional Value of Four Types of Egyptian Palm Pollens. J Pharm Nutr Sci. 2012;2(1):50–6. doi: 10.6000/1927-5951.2012.02.01.7

6. Vladimir-Knezevic S, Blazekovic MB, Stefan M, Babac M. Plant Polyphenols as Antioxidants Influencing the Human Health. In: Phytochemicals as Nutraceuticals—Global Approaches to Their Role in Nutrition and Health [Internet]. Dr Venkete. InTech; 2012. Available from: http://www.intechopen.com/books/phytochemicals-as-nutraceuticals-global-approaches-to-their-role-in-nutrition-and-health/plant-polyphenols-as-antioxidants-influencing-the-human-health. doi: 10.5772/27843

7. Aguiar J, Estevinho BN, Santos L. Microencapsulation of natural antioxidants for food application–The specific case of coffee antioxidants–A review. Trends Food Sci Technol [Internet]. 2016;58:21–39. Available from: http://dx.doi.org/10.1016/j.tifs.2016.10.012

8. de Souza Simões L, Madalena DA, Pinheiro AC, Teixeira JA, Vicente AA, Ramos ÓL. Micro- and nano bio-based delivery systems for food applications: In vitro behavior. Adv Colloid Interface Sci. 2017;243:23–45. doi: 10.1016/j.cis.2017.02.010 28395856

9. Rashidinejad A, Birch EJ, Sun-Waterhouse D, Everett DW. Effects of catechin on the phenolic content and antioxidant properties of low-fat cheese. Int J Food Sci Technol. 2013;48(12):2448–55. https://doi.org/10.1111/ijfs.12234

10. Haratifar S, Meckling KA, Corredig M. Antiproliferative activity of tea catechins associated with casein micelles, using HT29 colon cancer cells. J Dairy Sci [Internet]. 2014;97(2):672–8. Available from: http://linkinghub.elsevier.com/retrieve/pii/S002203021300859X doi: 10.3168/jds.2013-7263 24359816

11. Livney YD. Nanostructured delivery systems in food: Latest developments and potential future directions. Curr Opin Food Sci [Internet]. 2015;3:125–35. Available from: http://dx.doi.org/10.1016/j.cofs.2015.06.010

12. Katouzian I, Jafari SM. Nano-encapsulation as a promising approach for targeted delivery and controlled release of vitamins. Trends Food Sci Technol [Internet]. 2016;53:34–48. Available from: http://dx.doi.org/10.1016/j.tifs.2016.05.002

13. Estevinho BN, Rocha F, Santos L, Alves A. Microencapsulation with chitosan by spray drying for industry applications—A review. Trends Food Sci Technol. 2013;31:138–55. https://doi.org/10.1016/j.tifs.2013.04.001

14. AOAC International. Official methods of analysis. 20th ed. Latimer GW, editor. AOAC International, Rockville, Maryland 20850–3250, USA; 2016.

15. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem. 1956;28:350–6. https://doi.org/10.1021/ac60111a017

16. Beaty RD, Kerber JD. Concepts, Instrumentation and Techniques in Atomic Absorption Spectrophotometry. second Edi. North. The Perkin-Elmer Corporation, Norwalk, CT, U.S.A.; 1993.

17. Ling ER. A Textbook of Dairy Chemistry. 2nd ed. Vol. Two Practi. Chapman and Hall LTD, London; 1945.

18. Croci AN, Cioroiu B, Lazar D. HPLC evaluation of phenolic and polyphenolic acids from propolis. Farmacia. 2009;LVII(1):52–7. https://www.researchgate.net/publication/289758264

19. El-Neweshy MS, El-Maddawy ZK, El-Sayed YS. Therapeutic effects of date palm (Phoenix dactylifera L.) pollen extract on cadmium-induced testicular toxicity. Andrologia. 2013;45(6):369–78. doi: 10.1111/and.12025 22998418

20. Al-Owaisi M, Al-Hadiwi N, Khan SA. GC-MS analysis, determination of total phenolics, flavonoid content and free radical scavenging activities of various crude extracts of Moringa peregrina (Forssk.) Fiori leaves. Asian Pac J Trop Biomed [Internet]. 2014;4(12):964–70. Available from: http://www.researchpub.org/journal/ijfns/ijfns.html%5Cnhttp://dx.doi.org/10.1016/j.rser.2010.07.054%5Cnhttp://www.sciencedirect.com/science/article/pii/S222116911530112X

21. Vardhanabhuti B, Foegeding EA, McGuffey MK, Daubert CR, Swaisgood HE. Gelation properties of dispersions containing polymerized and native whey protein isolate. Food Hydrocoll. 2001;15(2):165–75. https://doi.org/10.1016/S0268-005X(00)00062-X

22. Munir H, Shahid M, Anjum F, Mudgil D. Structural, thermal and rheological characterization of modified Dalbergia sissoo gum-A medicinal gum. Int J Biol Macromol [Internet]. 2016;84:236–45. Available from: doi: 10.1016/j.ijbiomac.2015.12.001 26709145

23. Cerqueira MA, Souza BWS, Simoes J, Teixeira JA, Domingues MRM, Coimbra MA, et al. Structural and thermal characterization of galactomannans from non-conventional sources. Carbohydr Polym [Internet]. 2011;83(1):179–85. Available from: http://dx.doi.org/10.1016/j.carbpol.2010.07.036

24. Schumann K, Siekmann K. Soaps. In: IUllmann’s Encyclopedia of Industrial Chemistry. Weinheim: Wiley- VCH; 2000. p. 241–61.

25. Singleton VL, Orthofer R, Lamuela-Raventos RM. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteau reagent. Oxidants and antioxidants part A. Vol. 299, Methods in Enzymology. Academic Press; 1999. 152–178 p. https://doi.org/10.1016/S0076-6879(99)99017-1

26. Sakanaka S, Tachibana Y, Okada Y. Preparation and antioxidant properties of extracts of Japanese persimmon leaf tea (kakinoha-cha). Food Chem. 2005;9:569–75. https://doi.org/10.1016/j.foodchem.2004.03.013

27. Brand-Williams Cuvelier ME, Berset C. Use of a Free Radical Method to Evaluate Antioxidant Activity. Food Sci Technol. 1995;28:25–30. https://doi.org/10.1016/S0023-6438(95)80008-5

28. Mosmann T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1–2):55–63. doi: 10.1016/0022-1759(83)90303-4 6606682

29. Bassyouni FA, Abu-Baker SM, Mahmoud K, Moharam M, El-Nakkady SS, Abdel-Rehim M. Synthesis and biological evaluation of some new triazolo[1,5-a]quinoline derivatives as anticancer and antimicrobial agents. RSC Adv. 2014;4(46):24131–41.

30. Tamime AY, Robenson RK. Tamime and Robenson’s Yoghurt Science and Technology. 3rd ed. Cambridge England: Woodhead Publishing Ltd and CRC Press LLC; 2007. 808 p. eBook ISBN: 9781845692612

31. Hunter RS, Harold RW. The measurement of appearance [Internet]. 2nd Editio. A Wiley Interscience Publication, John Wiley & Sons. Inc; 1976. 421 p. Available from: http://physicstoday.scitation.org/doi/10.1063/1.3024412

32. Akalın AS, Unal G, Dinkci N, Hayaloglu AA. Microstructural, textural, and sensory characteristics of probiotic yogurts fortified with sodium calcium caseinate or whey protein concentrate. J Dairy Sci [Internet]. 2012;95(7):3617–28. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0022030212003426 doi: 10.3168/jds.2011-5297 22720919

33. Isanga J, Zhang G. Production and evaluation of some physicochemical parameters of peanut milk yoghurt. LWT—Food Sci Technol [Internet]. 2009;42(6):1132–8. Available from: http://dx.doi.org/10.1016/j.lwt.2009.01.014

34. Bourne MC. Food Texture and Viscosity: Concept and Measurement. 2nd ed. Elsevier Science & Technology Books; 2002.

35. Szczesniak AS. Classification of Textural Characteristics. J Food Sci. 1963;28(4):385–9. https://doi.org/10.1111/j.1365-2621.1963.tb00215.x

36. Marth EH. Standard Methods for the Examination of Dairy Products. 14th editi. American Public Health Association 1015 Eighteenth Street, N.W. Washington, DC 20036; 1978. 456 p.

37. Darwish AMG, Khalifa RE, El Sohaimy SA. Functional properties of chia seed mucilage supplemented in low fat yoghurt. Alexandria Sci Exch J. 2018;39(3):450–9. doi: 10.21608/ASEJAIQJSAE.2018.13882

38. Senaka Ranadheera C, Evans CA, Adams MC, Baines SK. Probiotic viability and physico-chemical and sensory properties of plain and stirred fruit yogurts made from goat’s milk. Food Chem [Internet]. 2012;135(3):1411–8. Available from: doi: 10.1016/j.foodchem.2012.06.025 22953874

39. Ozturk B, Argin S, Ozilgen M, McClements DJ. Nanoemulsion delivery systems for oil-soluble vitamins: Influence of carrier oil type on lipid digestion and vitamin D3 bioaccessibility. Food Chem. 2015;187:499–506. doi: 10.1016/j.foodchem.2015.04.065 25977056

40. ISO 22935–3 | IDF 099–3: 2009 –Milk and milk products–Sensory analysis–Part 3: Guidance on a method for evaluation of compliance with product specifications for sensory properties by scoring. First edit. ISO and IDF 2009; 2009. 7 p.

41. Hassan HMM. Chemical Composition and Nutritional Value of Palm Pollen Grains. Glob J Biotechnol Biochem. 2011;6(1):1–7.

42. Rasekh A, Jashni HK, Rahmanian K, Jahromi AS. Effect of palm pollen on sperm parameters of infertile man. Pakistan J Biol Sci. 2015;18(4):196–9. doi: 10.3923/pjbs.2015.196.199 26506651

43. Abed El-Azim MHM, Yassin FA, Khalil SA, Amani A, El-Mesalamy MD. Hydrocarbons, fatty acids and biological activity of date palm pollen (phoenix dactylifera L.) growing in Egypt. IOSR J Pharm Biol Sci Ver I [Internet]. 2015;10(3):2319–7676. Available from: www.iosrjournals.org doi: 10.9790/3008-10314651

44. Daoud A, Malika D, Bakari S, Hfaiedh N, Mnafgui K, Kadri A, et al. Assessment of polyphenol composition, antioxidant and antimicrobial properties of various extracts of Date Palm Pollen (DPP) from two Tunisian cultivars. Arab J Chem. 2015; https://doi.org/10.1016/j.arabjc.2015.07.014

45. Grzesik M, Naparło K, Bartosz G, Sadowska-Bartosz I. Antioxidant properties of catechins: Comparison with other antioxidants. Food Chem. 2018;241(June 2017):480–92. doi: 10.1016/j.foodchem.2017.08.117 28958556

46. Lima CF, Carvalho F, Fernandes E, Bastos ML, Santos-Gomes PC, Fernandes-Ferreira M, et al. Evaluation of toxic/protective effects of the essential oil of Salvia officinalis on freshly isolated rat hepatocytes. Toxicol In Vitro. 2004;18(4):457–65. doi: 10.1016/j.tiv.2004.01.001 15130603

47. Besbes S, Blecker C, Deroanne C, Drira NE, Attia H. Date seeds: Chemical composition and characteristic profiles of the lipid fraction. Food Chem. 2004;84(4):577–84. https://doi.org/10.1016/S0308-8146(03)00281-4

48. Simopoulos AP. Omega-6 / Omega-3 Essential Fatty Acid Ratio and Chronic Diseases. 2004;20(1):77–90. doi: 10.3181/0711-MR-311

49. Simopoulos AP. The importance of the ratio of omega-6 / omega-3 essential fatty acids. 2002;56:365–79. https://doi.org/10.1016/S0753-3322(02)00253-6 12442909

50. Pan K, Zhong Q, Baek SJ. Enhanced dispersibility and bioactivity of curcumin by encapsulation in casein nanocapsules. J Agric Food Chem. 2013;61(25):6036–43. doi: 10.1021/jf400752a 23734864

51. Rezaei A, Fathi M, Jafari SM. Nanoencapsulation of hydrophobic and low-soluble food bioactive compounds within different nanocarriers. Vol. 88, Food Hydrocolloids. Elsevier B.V.; 2019. 146–162 p. https://doi.org/10.1016/j.foodhyd.2018.10.003

52. Cho H, Lee HJ, Yu KS, Choi YM, Hwang KT. Characterisation and food application of curcumin bound to sodium caseinate–polysaccharide electrostatic complexes. Int J Food Sci Technol. 2017;52(8):1770–6. https://doi.org/10.1111/ijfs.13450

53. Almehdi AM, Maraqa M, Abdulkhalik S. Aerobiological studies and low allerginicity of Date-Palm pollen in the UAE. Int J Environ Health Res. 2005;15(3):217–24. doi: 10.1080/09603120500105745 16134484

54. Jazinizadeh E, Majd A, Pourpak Z. Anther development and microsporogenesis in date palm (Phoenix dactylifera L.) 2017;49(1):331–5.

55. Oladoja NA, Unuabonah EI, Amuda OS, Kolawole OM. Polysaccharides as a green and sustainable resources for water and wastewater treatment [Internet]. Cham, Switzerland: Springer Nature; 2017. Available from: http://link.springer.com/10.1007/978-3-319-56599-6

56. Farouk A, Metwaly A, Mohsen M. Chemical Composition and antioxidant activity of Date Palm pollen grains (Phoenix dactylifera L. Palmae) essential oil for Siwe Cultivar Cultivated in Egypt. Middle East J Appl Sci. 2015;5(4):945–9. https://www.researchgate.net/publication/320290100

57. Andersen FA. Final report on the safety assessment of lecithin and hydrogenated lecithin. Int J Toxicol. 2001;21(SUPPL. 2):21–45.

58. Jahromi AR, Jashni HK, Rahmanian K, Jahromi AS. Effect of palm pollen on sperm parameters of infertile man. Pakistan J Biol Sci. 2015;18(4):196–9.

59. Metry WA, Owayss AA. Influence of incorporating honey and royal jelly on the quality of yoghurt during storage. Egypt J Food Sci. 2009;37:115–31. https://www.researchgate.net/publication/283257408

60. Yerlikaya O. Effect of bee pollen supplement on antimicrobial, chemical, rheological, sensorial properties and probiotic viability of fermented milk beverages. Mljekarstvo [Internet]. 2014;64(4):268–79. Available from: http://hrcak.srce.hr/index.php?show=clanak&id_clanak_jezik=191970 https://doi.org/10.15567/mljekarstvo.2014.0406

61. Pichot R, Watson RL, Norton IT. Phospholipids at the interface: Current trends and challenges. Int J Mol Sci. 2013;14(6):11767–94. doi: 10.3390/ijms140611767 23736688

62. Puvanenthiran A, Williams RPW, Augustin MA. Structure and visco-elastic properties of set yoghurt with altered casein to whey protein ratios. Int Dairy J. 2002;12(4):383–91. https://doi.org/10.1016/S0958-6946(02)00033-X

63. Lucey JA. Formation and physical properties of milk protein gels. J Dairy Sci [Internet]. 2002;85(2):281–94. Available from: http://linkinghub.elsevier.com/retrieve/pii/S0022030202740782 https://doi.org/10.3168/jds.S0022-0302(02)74078- 11913691

64. Coggins PC, Rowe DE, Wilson JC, Kumari S. Storage and temperature effects on appearance and textural characteristics of conventional milk yogurt. J Sens Stud. 2010;25(4):549–76. https://doi.org/10.1111/j.1745-459X.2010.00286.x

65. de Souza Oliveira RP, Perego P, de Oliveira MN, Converti A. Effect of inulin on the growth and metabolism of a probiotic strain of Lactobacillus rhamnosus in co-culture with Streptococcus thermophilus. LWT—Food Sci Technol [Internet]. 2012;47(2):358–63. Available from: http://dx.doi.org/10.1016/j.lwt.2012.01.031

66. El-Kadi SL, Ismail MM, Zidan MS. Chemical and Microbial Characterizations of Bio-Yoghurt Made Using ABT Culture, Cow Milk and Coconut Milk. Ec Microbiol. 2017;5(3):109–24.

Článek vyšel v časopise


2019 Číslo 10