Research Article
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Bee bread boosts probiotic Yoghurt: Unveiling the impact on physiochemical, microbiological, and sensory attributes

Year 2024, , 471 - 480, 23.09.2024
https://doi.org/10.33988/auvfd.1326701

Abstract

This study aimed to investigate the effects of bee bread ratios of 0.5%, 1%, and 2%, respectively on some parameters in probiotic yoghurt production. The bee bread composition contained the elements B, Ca, Fe, K, Mg, Na, P, and Zn. The analysis of sugar composition revealed the presence of fructose, glucose, and sucrose. The organic acid and phenolic substance content were assessed. The following values were obtained: oxalic acid (1.26 mg/g), malic acid (7.79 mg/g), ascorbic acid (0.91 mg/g), citric acid (2.73 mg/g), p-coumaric acid (15.3 µg/g) and kaempferol (5.562.4 µg/g). The study determined the tocopherol content, specifically alpha (7.09 µg/g), beta (0.4 µg/g), gamma (0.77 µg/g), and delta (0.31 µg/g). A total of 55 distinct components were identified while analyzing the volatile and aroma profiles. This study found that the IC50 value of bee bread was 1.414 mg/mL. Bee bread did not affect physicochemical parameters such as pH, acidity, dry matter, ash, milk fat, and water holding capacity (P>0.05) but affected protein and syneresis (P<0.05). The addition of bee bread positively affected Streptococcus thermophilus and Lactobacillus bulgaricus, and Lactobacillus acidophilus LA-5 activity was preserved at around 107 kob/g during storage (P<0.05). Adding bee bread affected the color parameters L*, a*, and b* values (P<0.05). Consumers preferred the group to which 0.5% bee bread was offered following sensory analytical evaluation. The study has demonstrated that adding bee bread during yoghurt production can effectively maintain probiotic activity.

Supporting Institution

This research has been supported within the context of project no: 0770-DR-21/2017K12-41003 by The Scientific Research Projects Committee of Burdur Mehmet Akif Ersoy University.

Project Number

0770-DR-21

Thanks

This study was derived from the Ph.D. thesis of the first author.

References

  • Andjelkovic B, Jevtić G, Marković J, et al (2012): Quality of honey bee bread collected in spring. J Hyg Eng Des, 1, 275-277.
  • AOAC (2016): International Official Methods of Analysis. 20th ed. Latimer GW, editor. AOAC International, Rockville, Maryland 20850–3250, USA.
  • Atallah AA (2016): The production of bio-yoghurt with probiotic bacteria, royal jelly and bee pollen grains. J Nutr Food Sci, 6, 510.
  • Bakour M, Fernandes Â, Barros L, et al (2019): Bee bread as a functional product: Chemical composition and bioactive properties. LWT, 109, 276-282.
  • Bakour M, Laaroussi H, Ousaaid D, et al (2022): Bee bread as a promising source of bioactive molecules and functional properties: an up-to-date review. Antibiotics, 11, 203.
  • Barros L, Pereira E, Calhelha RC, et al (2013): Bioactivity and chemical characterization in hydrophilic and lipophilic compounds of Chenopodium ambrosioides L. J Funct Foods, 5, 1732-1740.
  • Bayram NE, Gercek YC, Çelik S, et al (2021): Phenolic and Free Amino Acid Profiles of Bee Bread and Bee Pollen with the Same Botanical Origin-Similarities and Differences. Arab J Chem, 14, 103004.
  • Canbulat Z, Ozcan T (2015): Effects of Short‐Chain and Long‐Chain Inulin on the Quality of Probiotic Yogurt Containing Lactobacillus rhamnosus. J Food Process Preserv, 39, 1251-1260.
  • Chr Hansen Technical Bulletin (2002): Method for counting Streptococcus thermophilus in Yoghurt - F-7. Technical Bulletin. Chr. Hansen Denmark.
  • Chr Hansen Technical Bulletin (2002): Method for counting Lactobacillus bulgaricus in Yoghurt - F-8. Technical Bulletin. Chr. Hansen Denmark.
  • Ćirić J, Haneklaus N, Rajić S, et al (2022): Chemical composition of bee bread (perga), a functional food: A review. J Trace Elem Med Biol, 2, 100038.
  • Coskun F, Karabulut Dirican L (2019): Effects of pine honey on the physicochemical, microbiological and sensory properties of probiotic yoghurt. Food Sci Technol Campinas, 39, 616-625.
  • Demirci T, Aktaş K, Sözeri D, et al (2017): Rice bran improve probiotic viability in yoghurt and provide added antioxidative benefits. J Funct Foods, 36, 396–403.
  • Dranca F, Ursachi F, Oroia M (2020): Bee Bread: Physicochemical Characterization and Phenolic Content Extraction Optimization. Foods, 9, 1358.
  • El-Kholy WM, Soliman TN, Darwish AMG (2019): Evaluation of date palm pollen (Phoenix dactylifera L.) encapsulation, impact on the nutritional and functional properties of fortified yoghurt. PLoS One, 14, e0222789.
  • Ghoreishy S, Shirzad N, Nakhjavani M, et al (2022): Effect of Daily Consumption of Probiotic Yoghurt on Albumin to Creatinine Ratio, Egfr and Metabolic Parameters In Patients With Type 2 Diabetes with Microalbuminuria: Study Protocol For A Randomised Controlled Clinical Trial. BMJ Open, 3, e056110.
  • Guarner F, Perdigón G, Corthier G, et al (2005): Should Yoghurt Cultures Be Considered Probiotic? Br J Nutr, 6, 783-786.
  • Habryka C, Kruczek M, Drygaś B (2016): Bee products used in apitherapy. World Sci News, 48, 254-258.
  • Hryniewicka M, Karpinska A, Kijewska M, et al (2016). LC/MS/MS analysis of α‐tocopherol and coenzyme Q10 content in lyophilized royal jelly, beebread and drone homogenate. J Mass Spectrom, 51, 1023-1029.
  • ISO - 20128 (2006): IDF 192, Milk products – Enumeration of presumptive Lactobacillus acidophilus on selective medium – Colony-count technique at 37 °C. Available at https://www.iso.org/standard/35292.html (Accessed July 12, 2023).
  • Ivanišová E, Kaˇcániová M, Franˇcáková H, et al (2015): Bee bread—Perspective source of bioactive compounds for future. Potravináestvo, 9, 592–598.
  • Ivey K, Hodgson J, Kerr D, et al (2015): The Effect of Yoghurt and Its Probiotics on Blood Pressure and Serum Lipid Profile; A Randomised Controlled Trial. Nutr Metab Cardiovasc Dis, 25, 46-51.
  • Kaplan M, Karaoglu Ö, Eroglu N, et al (2016): Fatty acid and proximate composition of bee bread. Food Technol Biotechnol, 54, 497-504.
  • Karabagias IK, Karabagias VK, Gatzias I, et al (2018): Bio-functional properties of bee pollen: The case of “bee pollen yoghurt”. Coatings, 8, 423-438.
  • Kaškonienė V, Venskutonis PR, Čeksterytė V (2008): Composition of volatile compounds of honey of various floral origin and beebread collected in Lithuania. Food Chem, 111, 988-997.
  • Khider M, Elbanna K, Mahmoud A, et al (2013): Egyptian honeybee pollen as antimicrobial, antioxidant agents, and dietary food supplements. Food Sci Biotechnol, 22, 1-9.
  • Kieliszek M, Piwowarek K, Kot A, et al (2018): Pollen and bee bread as new health-oriented products: A review. Trends Food Sci Technol, 71, 170-180.
  • Krapez KM, Abram V, Kac M, et al (2001): Determination of Organic Acids in White Wines by RP-HPLC. Food Technol Biotechnol, 39, 93-99.
  • Leon K, Mery D, Pedreschi F, et al (2006): Color measurement in L∗ a∗ b∗ units from RGB digital images. Food Res Int, 39, 1084-1091.
  • Mărgăoan R, Cornea-Cipcigan M, Topal E, et al (2020): Impact of fermentation processes on the bioactive profile and health-promoting properties of bee bread, mead and honey vinegar. Processes, 8, 1081.
  • Mărgăoan R, Stranț M, Varadi A, et al (2019): Bee collected pollen and bee bread: Bioactive constituents and health benefits. Antioxidants, 8, 568.
  • Miguel MDG, Doughmi O, Aazza S, et al (2014): Antioxidant, anti-inflammatory and acetylcholinesterase inhibitory activities of propolis from different regions of Morocco. Food Sci Biotechnol, 23, 313-322.
  • Morgano MA, Martins MCT, Rabonato LC, et al (2012): A comprehensive investigation of the mineral composition of Brazilian bee pollen: geographic and seasonal variations and contribution to human diet. J Braz Chem Soc, 23, 727-736.
  • Othman ZA, Noordin L, Ghazali WSW, et al (2019): Nutritional, phytochemical and antioxidant analysis of bee bread from different regions of Malaysia. Indian J Pharm Sci, 81, 955-960.
  • Ozcan M, Fındık S, Uylaşer V, et al (2020): Investigation of the Physical and Chemical Properties of Traditional Homemade Yogurt with Different Rates of Pollen Additions. EJOSAT, 20, 516-521.
  • Ozcan T, Yilmaz-Ersan L, Akpinar-Bayizit A, et al (2010): Viability of Lactobacillus acidophilus LA-5 and Bifidobacterium bifidum BB-12 in Rice Pudding. Mljekarstvo, 60, 135-144.
  • Panesar PS, Shinde C (2012): Effect of storage on syneresis, pH, Lactobacillus acidophilus count, Bifidobacterium bifidum count of Aloe vera fortified probiotic yoghurt. Curr Res Dairy Sci, 4, 17-23.
  • Sarkar S (2008): Effect Of Probiotics on Biotechnological Characteristics of Yoghurt. Br Food J, 110, 717-740.
  • Sobral F, Calhelha RC, Barros L, et al (2017): Flavonoid composition and antitumor activity of bee bread collected in northeast Portugal. Molecules, 22, 248-260.
  • Soliman N, Ahmed L (2019): Survival of Staphylococcus aureus in Bio-yoghurt. O J App S, 9, 564-572.
  • Tamime AY, Robinson RK (2007): Tamime and Robinson's Yoghurt: Science and Technology. 3rd ed. Woodhead Publishing Limited, Cambridge, UK.
  • Urcan A, Mărghıtaș LA, Dezmirean DS, et al (2017): Chemical Composition and Biological Activities of Beebread-Review. Bull Univ Agric Sci Vet Med Cluj Napoca, 74, 6-14.
  • Vásquez A, Olofsson TC (2009): The lactic acid bacteria involved in the production of bee pollen and bee bread. J Apic Res, 48, 189-195.
  • Veberic R, Trobec M, Herbinger K, et al (2005): Phenolic compounds in some apple (Malus domestica Borkh) cultivars of organic and integrated production. J Sci Food Agric, 85, 1687-1694.
  • Wang W, Bao Y, Hendricks GM, et al (2012): Consistency, microstructure and probiotic survivability of goats’ milk yoghurt using polymerized whey protein as a co-thickening agent. Int Dairy J, 24, 113-119.
  • Wu H, Hulbert GJ, Mount JR (2000): Effects of ultrasound on milk homogenization and fermentation with yogurt starter. Innov Food Sci Emerg Technol, 1, 211-218.
  • Yerlikaya O (2014): Effect of bee pollen supplement on antimicrobial, chemical, rheological, sensorial properties and probiotic viability of fermented milk beverages. Mljekarstvo, 64, 268-279.
Year 2024, , 471 - 480, 23.09.2024
https://doi.org/10.33988/auvfd.1326701

Abstract

Supporting Institution

Burdur Mehmet Akif Ersoy Üniversitesi Bilimsel Araştırma Projeleri Koordinatörlüğü

Project Number

0770-DR-21

References

  • Andjelkovic B, Jevtić G, Marković J, et al (2012): Quality of honey bee bread collected in spring. J Hyg Eng Des, 1, 275-277.
  • AOAC (2016): International Official Methods of Analysis. 20th ed. Latimer GW, editor. AOAC International, Rockville, Maryland 20850–3250, USA.
  • Atallah AA (2016): The production of bio-yoghurt with probiotic bacteria, royal jelly and bee pollen grains. J Nutr Food Sci, 6, 510.
  • Bakour M, Fernandes Â, Barros L, et al (2019): Bee bread as a functional product: Chemical composition and bioactive properties. LWT, 109, 276-282.
  • Bakour M, Laaroussi H, Ousaaid D, et al (2022): Bee bread as a promising source of bioactive molecules and functional properties: an up-to-date review. Antibiotics, 11, 203.
  • Barros L, Pereira E, Calhelha RC, et al (2013): Bioactivity and chemical characterization in hydrophilic and lipophilic compounds of Chenopodium ambrosioides L. J Funct Foods, 5, 1732-1740.
  • Bayram NE, Gercek YC, Çelik S, et al (2021): Phenolic and Free Amino Acid Profiles of Bee Bread and Bee Pollen with the Same Botanical Origin-Similarities and Differences. Arab J Chem, 14, 103004.
  • Canbulat Z, Ozcan T (2015): Effects of Short‐Chain and Long‐Chain Inulin on the Quality of Probiotic Yogurt Containing Lactobacillus rhamnosus. J Food Process Preserv, 39, 1251-1260.
  • Chr Hansen Technical Bulletin (2002): Method for counting Streptococcus thermophilus in Yoghurt - F-7. Technical Bulletin. Chr. Hansen Denmark.
  • Chr Hansen Technical Bulletin (2002): Method for counting Lactobacillus bulgaricus in Yoghurt - F-8. Technical Bulletin. Chr. Hansen Denmark.
  • Ćirić J, Haneklaus N, Rajić S, et al (2022): Chemical composition of bee bread (perga), a functional food: A review. J Trace Elem Med Biol, 2, 100038.
  • Coskun F, Karabulut Dirican L (2019): Effects of pine honey on the physicochemical, microbiological and sensory properties of probiotic yoghurt. Food Sci Technol Campinas, 39, 616-625.
  • Demirci T, Aktaş K, Sözeri D, et al (2017): Rice bran improve probiotic viability in yoghurt and provide added antioxidative benefits. J Funct Foods, 36, 396–403.
  • Dranca F, Ursachi F, Oroia M (2020): Bee Bread: Physicochemical Characterization and Phenolic Content Extraction Optimization. Foods, 9, 1358.
  • El-Kholy WM, Soliman TN, Darwish AMG (2019): Evaluation of date palm pollen (Phoenix dactylifera L.) encapsulation, impact on the nutritional and functional properties of fortified yoghurt. PLoS One, 14, e0222789.
  • Ghoreishy S, Shirzad N, Nakhjavani M, et al (2022): Effect of Daily Consumption of Probiotic Yoghurt on Albumin to Creatinine Ratio, Egfr and Metabolic Parameters In Patients With Type 2 Diabetes with Microalbuminuria: Study Protocol For A Randomised Controlled Clinical Trial. BMJ Open, 3, e056110.
  • Guarner F, Perdigón G, Corthier G, et al (2005): Should Yoghurt Cultures Be Considered Probiotic? Br J Nutr, 6, 783-786.
  • Habryka C, Kruczek M, Drygaś B (2016): Bee products used in apitherapy. World Sci News, 48, 254-258.
  • Hryniewicka M, Karpinska A, Kijewska M, et al (2016). LC/MS/MS analysis of α‐tocopherol and coenzyme Q10 content in lyophilized royal jelly, beebread and drone homogenate. J Mass Spectrom, 51, 1023-1029.
  • ISO - 20128 (2006): IDF 192, Milk products – Enumeration of presumptive Lactobacillus acidophilus on selective medium – Colony-count technique at 37 °C. Available at https://www.iso.org/standard/35292.html (Accessed July 12, 2023).
  • Ivanišová E, Kaˇcániová M, Franˇcáková H, et al (2015): Bee bread—Perspective source of bioactive compounds for future. Potravináestvo, 9, 592–598.
  • Ivey K, Hodgson J, Kerr D, et al (2015): The Effect of Yoghurt and Its Probiotics on Blood Pressure and Serum Lipid Profile; A Randomised Controlled Trial. Nutr Metab Cardiovasc Dis, 25, 46-51.
  • Kaplan M, Karaoglu Ö, Eroglu N, et al (2016): Fatty acid and proximate composition of bee bread. Food Technol Biotechnol, 54, 497-504.
  • Karabagias IK, Karabagias VK, Gatzias I, et al (2018): Bio-functional properties of bee pollen: The case of “bee pollen yoghurt”. Coatings, 8, 423-438.
  • Kaškonienė V, Venskutonis PR, Čeksterytė V (2008): Composition of volatile compounds of honey of various floral origin and beebread collected in Lithuania. Food Chem, 111, 988-997.
  • Khider M, Elbanna K, Mahmoud A, et al (2013): Egyptian honeybee pollen as antimicrobial, antioxidant agents, and dietary food supplements. Food Sci Biotechnol, 22, 1-9.
  • Kieliszek M, Piwowarek K, Kot A, et al (2018): Pollen and bee bread as new health-oriented products: A review. Trends Food Sci Technol, 71, 170-180.
  • Krapez KM, Abram V, Kac M, et al (2001): Determination of Organic Acids in White Wines by RP-HPLC. Food Technol Biotechnol, 39, 93-99.
  • Leon K, Mery D, Pedreschi F, et al (2006): Color measurement in L∗ a∗ b∗ units from RGB digital images. Food Res Int, 39, 1084-1091.
  • Mărgăoan R, Cornea-Cipcigan M, Topal E, et al (2020): Impact of fermentation processes on the bioactive profile and health-promoting properties of bee bread, mead and honey vinegar. Processes, 8, 1081.
  • Mărgăoan R, Stranț M, Varadi A, et al (2019): Bee collected pollen and bee bread: Bioactive constituents and health benefits. Antioxidants, 8, 568.
  • Miguel MDG, Doughmi O, Aazza S, et al (2014): Antioxidant, anti-inflammatory and acetylcholinesterase inhibitory activities of propolis from different regions of Morocco. Food Sci Biotechnol, 23, 313-322.
  • Morgano MA, Martins MCT, Rabonato LC, et al (2012): A comprehensive investigation of the mineral composition of Brazilian bee pollen: geographic and seasonal variations and contribution to human diet. J Braz Chem Soc, 23, 727-736.
  • Othman ZA, Noordin L, Ghazali WSW, et al (2019): Nutritional, phytochemical and antioxidant analysis of bee bread from different regions of Malaysia. Indian J Pharm Sci, 81, 955-960.
  • Ozcan M, Fındık S, Uylaşer V, et al (2020): Investigation of the Physical and Chemical Properties of Traditional Homemade Yogurt with Different Rates of Pollen Additions. EJOSAT, 20, 516-521.
  • Ozcan T, Yilmaz-Ersan L, Akpinar-Bayizit A, et al (2010): Viability of Lactobacillus acidophilus LA-5 and Bifidobacterium bifidum BB-12 in Rice Pudding. Mljekarstvo, 60, 135-144.
  • Panesar PS, Shinde C (2012): Effect of storage on syneresis, pH, Lactobacillus acidophilus count, Bifidobacterium bifidum count of Aloe vera fortified probiotic yoghurt. Curr Res Dairy Sci, 4, 17-23.
  • Sarkar S (2008): Effect Of Probiotics on Biotechnological Characteristics of Yoghurt. Br Food J, 110, 717-740.
  • Sobral F, Calhelha RC, Barros L, et al (2017): Flavonoid composition and antitumor activity of bee bread collected in northeast Portugal. Molecules, 22, 248-260.
  • Soliman N, Ahmed L (2019): Survival of Staphylococcus aureus in Bio-yoghurt. O J App S, 9, 564-572.
  • Tamime AY, Robinson RK (2007): Tamime and Robinson's Yoghurt: Science and Technology. 3rd ed. Woodhead Publishing Limited, Cambridge, UK.
  • Urcan A, Mărghıtaș LA, Dezmirean DS, et al (2017): Chemical Composition and Biological Activities of Beebread-Review. Bull Univ Agric Sci Vet Med Cluj Napoca, 74, 6-14.
  • Vásquez A, Olofsson TC (2009): The lactic acid bacteria involved in the production of bee pollen and bee bread. J Apic Res, 48, 189-195.
  • Veberic R, Trobec M, Herbinger K, et al (2005): Phenolic compounds in some apple (Malus domestica Borkh) cultivars of organic and integrated production. J Sci Food Agric, 85, 1687-1694.
  • Wang W, Bao Y, Hendricks GM, et al (2012): Consistency, microstructure and probiotic survivability of goats’ milk yoghurt using polymerized whey protein as a co-thickening agent. Int Dairy J, 24, 113-119.
  • Wu H, Hulbert GJ, Mount JR (2000): Effects of ultrasound on milk homogenization and fermentation with yogurt starter. Innov Food Sci Emerg Technol, 1, 211-218.
  • Yerlikaya O (2014): Effect of bee pollen supplement on antimicrobial, chemical, rheological, sensorial properties and probiotic viability of fermented milk beverages. Mljekarstvo, 64, 268-279.
There are 47 citations in total.

Details

Primary Language English
Subjects Veterinary Food Hygiene and Technology
Journal Section Research Article
Authors

Nilay Keyvan 0000-0002-6717-2793

Ozen Yurdakul 0000-0001-7680-015X

Project Number 0770-DR-21
Early Pub Date March 19, 2024
Publication Date September 23, 2024
Published in Issue Year 2024

Cite

APA Keyvan, N., & Yurdakul, O. (2024). Bee bread boosts probiotic Yoghurt: Unveiling the impact on physiochemical, microbiological, and sensory attributes. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 71(4), 471-480. https://doi.org/10.33988/auvfd.1326701
AMA Keyvan N, Yurdakul O. Bee bread boosts probiotic Yoghurt: Unveiling the impact on physiochemical, microbiological, and sensory attributes. Ankara Univ Vet Fak Derg. September 2024;71(4):471-480. doi:10.33988/auvfd.1326701
Chicago Keyvan, Nilay, and Ozen Yurdakul. “Bee Bread Boosts Probiotic Yoghurt: Unveiling the Impact on Physiochemical, Microbiological, and Sensory Attributes”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71, no. 4 (September 2024): 471-80. https://doi.org/10.33988/auvfd.1326701.
EndNote Keyvan N, Yurdakul O (September 1, 2024) Bee bread boosts probiotic Yoghurt: Unveiling the impact on physiochemical, microbiological, and sensory attributes. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71 4 471–480.
IEEE N. Keyvan and O. Yurdakul, “Bee bread boosts probiotic Yoghurt: Unveiling the impact on physiochemical, microbiological, and sensory attributes”, Ankara Univ Vet Fak Derg, vol. 71, no. 4, pp. 471–480, 2024, doi: 10.33988/auvfd.1326701.
ISNAD Keyvan, Nilay - Yurdakul, Ozen. “Bee Bread Boosts Probiotic Yoghurt: Unveiling the Impact on Physiochemical, Microbiological, and Sensory Attributes”. Ankara Üniversitesi Veteriner Fakültesi Dergisi 71/4 (September 2024), 471-480. https://doi.org/10.33988/auvfd.1326701.
JAMA Keyvan N, Yurdakul O. Bee bread boosts probiotic Yoghurt: Unveiling the impact on physiochemical, microbiological, and sensory attributes. Ankara Univ Vet Fak Derg. 2024;71:471–480.
MLA Keyvan, Nilay and Ozen Yurdakul. “Bee Bread Boosts Probiotic Yoghurt: Unveiling the Impact on Physiochemical, Microbiological, and Sensory Attributes”. Ankara Üniversitesi Veteriner Fakültesi Dergisi, vol. 71, no. 4, 2024, pp. 471-80, doi:10.33988/auvfd.1326701.
Vancouver Keyvan N, Yurdakul O. Bee bread boosts probiotic Yoghurt: Unveiling the impact on physiochemical, microbiological, and sensory attributes. Ankara Univ Vet Fak Derg. 2024;71(4):471-80.