THE EFFECT OF CHLORELLA VULGARIS ADDITION ON BREAD QUALITY CRITERIA

Öz

The utilisation of microalgae as a food source in the development of new and functional products, such as gluten-free bread with low nutritional value, is a subject of considerable interest. This is due to the nutritional components of microalgae, which include protein, fatty acids, minerals, vitamins, phenolics and antioxidants. The present study investigates the physicochemical, functional and sensory properties of corn bread (CME) produced by adding Chlorella vulgaris to corn flour at 1, 3, 6 and 10% ratios. The findings revealed that Chlorella addition led to an enhancement in protein, ash, fat, water holding capacity, and antioxidant values, accompanied by a reduction in moisture, volume, and sensory parameters. In the sensory evaluation, the control bread received the highest scores, while the specific colour, odour and taste of Chlorella decreased consumer acceptability. CME-10, the most nutritionally rich sample, was statistically significantly higher than the control sample in terms of total phenolics (extractable, hydrolyzable) and antioxidant capacity (ABTS, CUPRAC and DPPH) with high mineral and protein content.

Anahtar Kelimeler

• microalgae
• corn bread
• quality criteria

CHLORELLA VULGARİS İLAVESİNİN EKMEK KALİTE KRİTERLERİ ÜZERİNE ETKİSİ

Öz

Mikroalgler, protein, yağ asitleri, mineral, vitamin, fenolik ve antioksidan gibi besinsel bileşenleri sayesinde düşük besin değerine sahip glütensiz ekmek gibi yeni ve fonksiyonel ürünlerin geliştirilmesinde bir besin kaynağı olarak kullanılabilmektedir. Bu çalışmada, mısır ununa %1, 3, 6 ve 10 oranlarında Chlorella vulgaris ilave edilerek üretilen mısır ekmeklerinin (CME) fizikokimyasal, fonksiyonel ve duyusal özellikleri incelenmiştir. Chlorella ilavesi, protein, kül, yağ, su tutma kapasitesi ve antioksidan değerlerinde artışa, nem, hacim ve duyusal parametrelerde ise azalmaya neden olmuştur. Duyusal değerlendirmede kontrol ekmeği en yüksek puanları alırken, Chlorella’nın kendine has rengi, kokusu ve tadı tüketici kabul edilebilirliğini düşürmüştür. Besinsel olarak en zengin örnek olan CME-10, yüksek mineral ve protein içeriği ile toplam fenolik madde (ekstrakte edilebilir, hidrolize edilebilir) ve antioksidan kapasite (ABTS, CUPRAC ve DPPH) açısından kontrol örneğinden istatistiksel olarak önemli düzeyde yüksek belirlenmiştir.

Anahtar Kelimeler

• mikroalg
• mısır ekmeği
• kalite kriterleri

Kaynakça

1. AACC (2015). Approved methods of American Association of Cereal Chemists International (11th ed.). St. Paul, MN, USA.
2. Abdel-Karim, O. H., Gheda, S. F., Ismail, G. A., Abo-Shady, A. M. (2019). Phytochemical Screening and antioxidant activity of Chlorella vulgaris. Delta Journal of Science, 41(1), 79-91.
3. Adal, S. (2018). Yumurta kabuğu tozu kullanılarak mineral madde bakımından zenginleştirilen ekmeklerin bazı fiziksel ve kimyasal özelliklerinin belirlenmesi (Yüksek lisans tezi). Manisa Celal Bayar Üniversitesi, Fen Bilimleri Enstitüsü, Manisa.
4. Ahmed, H., Kumar, P. (2022). Effect of high-pressure treatment on oscillatory rheology, particle size distribution and microstructure of microalgae Chlorella vulgaris and Arthrospira platensis. Algal Research, 62: 102617.
5. Anonim, (2003). Danish food composition databank. Erişim: 05 Mayıs 2018. http://www.foodcomp.d
6. Apak, R., Güçlü, K., Özyürek, M., Karademir, S.E. (2004). Novel total antioxidant capacity index for dietary polyphenols and vitamins C and E, using their cupric ion reducing capability in the presence of neocuproine: CUPRAC method. Journal of Agricultural and Food Chemistry, 52(26): 7970–7981.
7. Apak, R., Güçlü, K., Özyürek, M., Esin, M. (2008). Mechanism of antioxidant capacity assays and the CUPRAC (cupric ion reducing antioxidant capacity) assay. Microchimica Acta, 160(4): 413–419.
8. Arendt, E.K., Dal Bello, F. (Eds.). (2008). Gluten-free cereal products and beverages. London: Academic Press.

9. Argun, M. Ş. (2016). Ülkemizde yetiştirilen bazı mısır çeşitlerine uygulanan alkali pişirme işleminin mısır unlarının karakteristik özellikleri üzerine etkilerinin araştırılması. (Doktora tezi).
10. Batista, A.P., Gouveia, L., Bandarra, N.M., Franco, J.M., Raymundo, A. (2013). Comparison of microalgal biomass profiles as novel functional ingredient for food products. Algal Research, 2(2): 164–173.
11. Batista, A.P., Niccolai, A., Biondi, N., Rodolfi, L., D’Ottavio, M., Tredici, M.R. (2017). Microalgae as potential sources of high-value compounds for food and feed. Journal of Applied Phycology, 29(3): 1357–1372.
12. Becker, E.W. (2007). Micro-algae as a source of protein. Biotechnology Advances, 25(2): 207–210.
13. Belorio, M., Gómez, M. (2020). Effect of hydration on gluten-free breads made with hydroxypropyl methylcellulose in comparison with psyllium and xanthan gum. Foods, 9(11): 1548.
14. Bledsoe, A.C., King, K.S., Larson, J.J., Snyder, M., Absah, I., Choung, R.S., Murray, J.A. (2019). Micronutrient deficiencies are common in contemporary celiac disease despite lack of overt malabsorption symptoms. Mayo Clinic Proceedings, 94(7): 1253–1260.
15. Bourvellec, L.B., Renard, C.M.G.C. (2012). Interactions between polyphenols and macromolecules: Quantification methods and mechanisms. Critical Reviews in Food Science and Nutrition, 52(3): 213–248.
16. Brand-Williams, W., Cuvelier, M. E., Berset, C. (1995). Use of a free radical method to evaluate antioxidant activity. LWT - Food Science and Technology, 28(1), 25–30.
17. Capocchi, A., Bottega S, Spanò C, Fontanini D. (2017). Phytochemicals and antioxidant capacity in four Italian traditional maize (Zea mays L.) varieties. International Journal of Food Science and Nutrition, 68(5): 515-524.
18. Caporgno, M. ve Mathys, A. (2018). Trends in microalgae incorporation into innovative food products with potential health benefits. Frontiers in Nutrition, 5.
19. Capriles, V.D., Arêas, J.A.G. (2014). Novel approaches in gluten-free breadmaking: Interface between food science, nutrition, and health. Comprehensive Reviews in Food Science and Food Safety, 13(5): 871–890.
20. Culetu, A., Susman, I. E., Duta, D. E., Belc, N. (2021). Nutritional and functional properties of gluten-free flours. Applied Sciences, 11(14), 6283.
21. Çelik, İ., Gökmen, V. (2018). Impact of thermal processing on total phenolic and antioxidant capacities of whole grain cereals. Journal of Cereal Science, 81: 55–60.
22. Dantas, D., Cahú, T., Oliveira, C., Abadie‐Guedes, R., Roberto, N., Santana, W., Bezerra, R. (2021). Chlorella vulgaris functional alcoholic beverage: effect on propagation of cortical spreading depression and functional properties. Plos One, 16(8), e0255996.
23. Demirkesen, I., Ozkaya, B. (2022). Recent strategies for tackling the problems in gluten-free diet and products. Critical Reviews in Food Science and Nutrition, 62(3): 571–597.
24. Deng, G.F., Xu, X.R., Guo, Y.J., Xia, E.Q., Li, S., Wu, S., Chen, F., Ling, W.H., Li, H.B. (2012). Determination of antioxidant property and their lipophilic and hydrophilic phenolic contents in cereal grains. Journal of Functional Foods, 4, 906-914.
25. Deora, N.S., Deswal, A., Mishra, H.N. (2014). Alternative approaches towards gluten-free dough development: Recent trends. Food Engineering Reviews, 6(3): 89–104.
26. Dewettinck, K., Van Bockstaele, F., Kuhne, B., Van de Walle, D., Courtens, T.M., Gellynck, X. (2008). Nutritional value of bread: Influence of processing, food interaction, and consumer perception. Journal of Cereal Science, 48(2): 243–257.
27. Diprat, A.B., Silveira Thys, R.C., Rodrigues, E., Rech, R. (2020). Chlorella sorokiniana: A new alternative source of carotenoids and proteins for gluten-free bread. LWT, 134: 110020.
28. Dündar, A., Şahin, O., Sarıcaoğlu, F. (2023). Low-fat cookies with chlorella vulgaris: effects on dough rheology, physical, textural and sensory properties of cookies. Gida / the Journal of Food, 48(3), 526-544.
29. El Khoury, D., Balfour-Ducharme, S., Joye, I.J. (2018). A review on the gluten-free diet: Technological and nutritional challenges. Nutrients, 10(10): 1410.
30. Freitas, M., Ferreira, J., Nunes, M., Raymundo, A. (2023). The chemistry and bioactive properties behind microalgae‐enriched gluten‐free breads. International Journal of Food Science & Technology, 59(2), 872-885.
31. Foschia, M., Horstmann, S., Arendt, E.K., Zannini, E. (2016). Nutritional therapy—Facing the gap between coeliac disease and gluten-free food. International Journal of Food Microbiology, 239: 113–124.
32. Fradique, M., Batista, A.P., Nunes, M.C., Gouveia, L., Bandarra, N.M., Raymundo, A. (2010). Incorporation of Chlorella vulgaris and Spirulina maxima biomass in pasta products. Journal of the Science of Food and Agriculture, 90(10): 1656–1664.
33. Garcia-Segovia, P., Andrés-Bello, A., Martínez-Monzó, J. (2007). Effect of cooking method on mechanical properties, color, and structure of beef muscle (M. pectoralis). Journal of Food Engineering, 181: 64–72.
34. Garzon, R., Skendi, A., Antonio Lazo-Velez, M., Papageorgiou, M., Rosell, C. M. (2021). Interaction of dough acidity and microalga level on bread quality and antioxidant properties. Food Chemistry, 344.
35. Gouveia, L., Batista, A.P., Miranda, A., Empis, J., Raymundo, A. (2007). Chlorella vulgaris biomass used as colouring source in traditional butter cookies. Innovative Food Science & Emerging Technologies, 8(3): 433–436.
36. Graça, C., Fradinho, P., Sousa, I. Raymundo, A. (2018). Impact of Chlorella vulgaris on the rheology of wheat flour dough and bread texture. LWT-Food Science and Technology, 89 (November 2017), 466–474. Green, P.H., Lebwohl, B., Greywoode, R. (2015). Celiac disease. Journal of Allergy and Clinical Immunology, 135(5): 1099–1106.
37. Güdük, H. (2016). Mısırlı ekmeklerde mısır unu seviyesi ve katkı kullanımının kalite üzerine etkisi. Atatürk Üniversitesi Fen Bilimleri Enstitüsü Gıda Mühendisliği Anabilim Dalı Yüksek Lisans Tezi, Erzurum, 104 s.
38. Gwirtz, J.A., Garcia-Casal, M.N. (2014). Processing maize flour and corn meal food products. Annals of the New York Academy of Sciences, 1312(1): 66–75.
39. Hager, A.S., Arendt, E.K. (2013). Influence of hydroxypropylmethylcellulose (HPMC), xanthan gum and their combination on loaf specific volume, crumb hardness and crumb grain characteristics of gluten-free breads based on rice, maize, teff and buckwheat. Food Hydrocolloids, 32(1): 195–203.
40. Holtmeier, W., Caspary, W.F. (2006). Celiac disease. Orphanet Journal of Rare Diseases, 1(1): 3.
41. Kahraman, G. (2016). Development of gluten-free bread formulations based on chickpea flour: Optimization of formulation, evaluation of dough properties and bread quality. Unpublished doctoral dissertation, İzmir Institute of Technology, İzmir, Turkey
42. Karabulut, I., Yemiş, O. (2019). Fenolik Bileşiklerin Bağlı Formları ve Biyoyararlılığı. Akademik Gıda, 17 (4): 526-537. Kelly, C.P., Bai, J.C., Liu, E., Leffler, D.A. (2015). Advances in diagnosis and management of celiac disease. Gastroenterology, 148(6): 1175–1186.
43. Khemiri, S., Khelifi, N., Nunes, M. C., Ferreira, A., Gouveia, L., Smaali, I., Raymundo, A. (2020). Microalgae biomass as an additional ingredient of gluten-free bread: Dough rheology, texture quality and nutritional properties. Algal Research, 50, 101998.
44. Kılınççeker, O., Hepsağ, F. (2010). Kaplama malzemesi olarak mısır unlarının bazı kalite özelliklerinin belirlenmesi. Gıda Teknolojileri Elektronik Dergisi, 5(2): 20–27.
45. Köten, H., Ünsal, A.M. (2021). Mısır unu ilavesinin pandispanya tipi keklerin morfogeometrik, fonksiyonel ve tekstürel özelliklerine etkisi. Harran Tarım ve Gıda Bilimleri Dergisi, 25(2): 172-184.
46. Kulp K, Ponte Jr J.G (Eds.), (2000), Handbook of cereal science and technology (2nd Ed.), Marcel Dekker, New York, USA, 1-30.
47. Lopes, A.P., Santos, F.M., Silva, T.F.C.V., Vilar, V.J.P., Pires, J.C.M. (2020). Outdoor cultivation of the microalga Chlorella vulgaris in a new photobioreactor configuration: The effect of ultraviolet and visible radiation. Energies, 13(8): 1962.
48. Ludvigsson, J.F., Murray, J.A. (2019). Epidemiology of celiac disease. Gastroenterology Clinics of North America, 48(1): 1-18.
49. Machado, A., Pereira, H., Costa, M., Santos, T., Carvalho, B., Soares, M., Silva, J. (2020). Development of an organic culture medium for autotrophic production of Chlorella vulgaris biomass. Applied Sciences, 10(6): 2156.
50. Mahmoud, N., Ferreira, J., Raymundo, A., Nunes, M. (2024). Enhancing the protein, mineral content, and bioactivity of wheat bread through the utilisation of microalgal biomass: a comparative study of chlorella vulgaris, phaeodactylum tricornutum, and tetraselmis chuii. Applied Sciences, 14(6), 2483.
51. Martinez, M.M., Gómez, M. (2017). Rheological and microstructural evolution of the most common gluten-free flours and starches during bread fermentation and baking. Journal of Food Engineering, 197, 78–86.
52. Matos, M.E., Rosell, C.M. (2015). Understanding gluten-free dough for reaching breads with physical quality and nutritional balance. Journal of the Science of Food and Agriculture, 95(4): 653–661.
53. Molino, A.M., Miccio, G., Iovine, A., Marino, T., Musmarra, D. (2018). Microalgae characterization for consolidated and new application in human food, animal feed and nutraceuticals. International Journal of Environmental Research and Public Health, 15 (11), 1–21.
54. Naczk, M., Shahidi, F. (2006). Phenolics in cereals, fruits and vegetables: Occurrence, extraction and analysis. Journal of Pharmaceutical and Biomedical Analysis, 41(5): 1523–1542.
55. Nuss, E.T., Tanumihardjo, S.A. (2010). Maize: A paramount staple crop in the context of global nutrition. Comprehensive Reviews in Food Science and Food Safety, 9(4): 417–436.
56. Panahi, Y., Darvishi, B., Sahebkar, A., Jowzi, N., Beiraghdar, F., Tayarani-Najaran, Z. (2016). Chlorella vulgaris: A multifunctional dietary supplement with diverse medicinal properties. Current Pharmaceutical Design, 22(2): 164-173.
57. Pereira, T., Barroso, S., Pinto, F., Silva, F., Teixeira, P., Mendes, S., Gil, M. (2024). Application of microalgae as natural colorant for pastry and confectionary products. Food Science & Nutrition, 12(11), 9479-9492.
58. Pérez-Jiménez, J., Saura-Calixto, F. (2015). Macromolecular antioxidants or non-extractable polyphenols in fruit and vegetables: Intake in four European countries. Food Research International, 74, 315-323.
59. Qazi, W. M., Ballance, S., Kousoulaki, K., Uhlen, A. K., Kleinegris, D. M. M., Skjånes, K., Rieder, A. (2021). Protein enrichment of wheat bread with microalgae: Microchloropsis Gaditana, Tetraselmis Chui and Chlorella Vulgaris. Foods, 10 (12).
60. Qazi, M. W., de Sousa, I. G., Nunes, M. C., Raymundo, A. (2022). Improving the nutritional, structural, and sensory properties of gluten-free bread with different species of microalgae. Foods, 11 (3).
61. Rybicka, I., Gliszczy-Swiglio, A. (2017). Minerals in grain gluten-free products. The content of calcium, potassium, magnesium, sodium, copper, iron, manganese, and zinc. Journal of Food Composition and Analysis, 59, 61–67.
62. Sabanis, D., Tzia, C. (2011). Effect of hydrocolloids on selected properties of gluten-free dough and bread. Food Science and Technology International, 17(4): 279–291.
63. Safafar, H., Van Wagenen, J., Møller, P., Jacobsen, C. (2015). Microalgal carotenoids: A review of production, extraction, stability, and bioaccessibility. Marine Drugs, 13(9): 5462–5487.
64. Safavi, N., Gharekhani, M. (2019). The effect of sodium caseinate and microbial transglutaminase enzyme on rheological, physical, and sensorial properties of corn-based gluten-free bread. Journal of Research and Innovation in Food Science and Technology, 7(4): 365–376.
65. Sahni, P., Sharma, S., Singh, B. (2019). Evaluation and quality assessment of defatted microalgae meal of Chlorella as an alternative food ingredient in cookies. Nutrition and Food Science, 49 (2), 221–231.
66. Schüler, L., Morais, E., Trovão, M., Machado, A., Carvalho, B., Carneiro, M., … ve Varela, J. (2020). Isolation and characterization of novel chlorella vulgaris mutants with low chlorophyll and improved protein contents for food applications. Frontiers in Bioengineering and Biotechnology, 8.
67. Scieszka, S. ve Klewicka, E. (2020). Influence of the microalga chlorella vulgaris on the growth and metabolic activity of Lactobacillus spp. bacteria. Foods, 9(7), 959.
68. Simić, M., Žilić, S., Šimuruna, O., Filipčev, B., Škrobot, D., Vančetović, J. (2018). Effects of anthocyanin-rich popping maize flour on the phenolic profile and the antioxidant capacity of mix-bread and its physical and sensory properties. Polish Journal of Food and Nutrition Sciences, 68(4): 299–308.
69. Singh, N., Singh, S., Shevkani, K. (2019). Maize: Composition, bioactive constituents, and unleavened bread. Flour and Breads and Their Fortification in Health and Disease Prevention, 111–121.
70. Sit, N., Misra, S., Deka, S. C. (2013). ‘Physicochemical, functional, textural and colour characteristics of starches isolated from four taro cultivars of north-east India’’, Starch-Stärke, 65: (11-12), 1011-1021.
71. Suri, D.J., Tanumihardjo, S.A. (2016). Effects of different processing methods on the micronutrient and phytochemical contents of maize: from A to Z. Comprehensive Reviews in Food Science and Food Safety, 15 (5), 912–926.
72. Tian, S., Wang, F., Luo, M., Yan, F., Ke, D., Chen, H., Gao, S. (2022). Effect of Chlorella pyrenoidosa powder on rheological properties and fermentation characteristics of dough. Journal of Food Processing and Preservation, 46 (4), 1–10.
73. Tibbetts, S. M., MacPherson, T., McGinn, P. J., Fredeen, A. H. (2016). In vitro digestion of microalgal biomass from freshwater species isolated in Alberta, Canada for monogastric and ruminant animal feed applications. Algal Research, 19, 324–332.
74. Torrinha, Á., Oliveira, M., Marinho, S., Paíga, P., Delerue-Matos, C. Simone, M. (2019). Mineral Content of Various Portuguese Breads: Characterization, Dietary Intake, and Discriminant Analysis. Molecules, 24 (2787).
75. Trehan, S., Singh, N., Kaur, A. (2018). Characteristics of white, yellow, purple corn accessions: phenolic profile, textural, rheological properties and muffin making potential. Journal of Food Science and Technology, 55 (6), 2334–2343.
76. Tümer, E., Özer, S. (2018). Bazı fonksiyonel ürünlerin glutensiz ekmek üretiminde ekmek nitelikleri üzerine etkisi. Çukurova Üniversitesi Fen ve Mühendislik Bilimleri Dergisi, 36: 6.
77. Uribe-Wandurraga, Z. N., Igual, M., García-Segovia, P., Martínez-Monzó, J. (2020a). In vitro bioaccessibility of minerals from microalgae-enriched cookies. Food and Function, 11 (3), 2186–2194.
78. Uribe-Wandurraga, Z. N., Igual, M., Reino-Moyón, J., García-Segovia, P., Martínez-Monzó, J. (2020b). Effect of microalgae (Arthrospira platensis and Chlorella vulgaris) addition on 3D printed cookies. Food Biophysics, 16 (1), 27–39.
79. Vitali, D., Dragojević, I. V., Šebečić, B. (2009). Effects of incorporation of integral raw materials and dietary fibre on the selected nutritional and functional properties of biscuits. Food Chemistry, 114 (4), 1462–1469.
80. Wandersleben, T., Morales, E., Burgos-Diaz, C., Barahona, T., Labra, E., Rubilar, M., Salvo-Garrido, H. (2018). Enhancement of functional and nutritional properties of bread using a mix of natural ingredients from novel varieties of flaxseed and lupine. LWT – Food Science and Technology, 91: 48–54.
81. Wazed, M. A., Islam, M. R. (2021). Influence of barley, corn and rice flour on physical, chemical and sensory characteristics of gluten-free bread. Malaysian Journal of Halal Research, 4 (2), 36–41.
82. Yılmaz, V.A. (2017). Hamsi unu ile zenginleştirilen mısır ekmeğinin özellikleri ve raf ömrünün belirlenmesi (Doktora tezi). Ondokuz Mayıs Üniversitesi, Fen Bilimleri Enstitüsü, Samsun.