Trends in Microalgae Incorporation Into Innovative Food Products With Potential Health Benefits

Frontiers in Nutrition

Volumn 5, Issue , 2018, Pages

  Caporgno, Martín P ^a   Mathys, Alexander ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

bioactive compounds; innovative food products; microalgae; peptides; proteins

Indexed keywords

EID: 85056132978     PISSN: None     EISSN: 2296861X     Source Type: Journal    
DOI: 10.3389/fnut.2018.00058     Document Type: Review

References (95)

1. United Nations Department of Economic and Social Affairs. World Population Projected to Reach 9.8 Billion in 2050, and 11.2 Billion in 2100 (2017). Available online at: https://www.un.org/development/desa/en/news/population/world-population-prospects-2017.html (Accessed March 19, 2018).
2. Sixty-fourth General Assembly United Nations. Food Production Must Double by 2050 to Meet Demand from World's Growing Population, Innovative Strategies Needed to Combat Hunger, Experts Tell Second Committee (2009). Available online at: https://www.un.org/press/en/2009/gaef3242.doc.htm (Accessed March 19, 2018).
3. Wijnands J, van der Meulen B, Poppe K. Competitiveness of the European Food Industry: An Economic and Legal Assessment 2007. The Hague: Office for Official Publications of the European Communities (2006).
4. Wu G, Fanzo J, Miller DD, Pingali P, Post M, Steiner JL, Thalacker-Mercer AE. Production and supply of high-quality food protein for human consumption: sustainability, challenges, and innovations. Ann N Y Acad. Sci. (2014) 1321:1–19. 10.1111/nyas.1250025123207
5. Tukker A, Jansen B. Environmental impacts of products: a detailed review of studies. ? J Ind Ecol. (2006) 10:159–82. 10.1162/jiec.2006.10.3.159
6. Vermeulen SJ, Campbell BM, Ingram JSI. Climate change and food systems. Annu Rev Environ Resour. (2012) 37:195–222. 10.1146/annurev-environ-020411-130608
7. Häusling M. The EU Protein Deficit: What Solution for a Long-standing Problem. European Parliament. Strasbourg: European Parliament 2010/2011 (2011).
8. Smetana S, Mathys A, Knoch A, Heinz V. Meat alternatives: life cycle assessment of most known meat substitutes. Int J Life Cycle Assess. (2015) 20:1254–67. 10.1007/s11367-015-0931-6
9. Chaudhary A, Gustafson D, Mathys A. Multi-indicator sustainability assessment of global food systems. Nat Commun. (2018) 9:848. 10.1038/s41467-018-03308-729487286
10. Meier T. Umweltschutz mit Messer und Gabel. Der ökologische Rucksack der Ernährung in Deutschland. München: Oekom Verlag (2013).
11. Pimentel D, Pimentel M. Sustainability of meat-based and plant-based diets and the environment. Am J Clin Nutr. (2003) 78:660S−3S. 10.1093/ajcn/78.3.660S12936963
12. Rosi A, Mena P, Pellegrini N, Turroni S, Neviani E, Ferrocino I, et al. Environmental impact of omnivorous, ovo-lacto-vegetarian, and vegan diet. Sci Rep. (2017) 7:6105. 10.1038/s41598-017-06466-828733610
13. Behrens P, Kiefte-de Jong JC, Bosker T, Rodrigues JFD, de Koning A, Tukker A. Evaluating the environmental impacts of dietary recommendations. Proc Natl Acad Sci USA. (2017) 114:13412–7. 10.1073/pnas.171188911429203655
14. FAO. World Agriculture: Towards 2015/2030, Summary Report (2002). Available online at: http://www.fao.org/docrep/004/Y3557E/y3557e03.htm (Accessed March 19, 2018).
15. FAO. Protein Sources for the Animal Feed Industry (2004). Available at: http://www.fao.org/docrep/007/y5019e/y5019e03.htm (Accessed March, 2018).
16. van der Spiegel M, Noordam MY, van der Fels-Klerx HJ. Safety of novel protein sources (insects, microalgae, seaweed, duckweed, and rapeseed) and legislative aspects for their application in food and feed production. Compr Rev Food Sci Food Saf. (2013) 12:662–78. 10.1111/1541-4337.12032
17. Spolaore P, Joannis-Cassan C, Duran E, Isambert A. Commercial applications of microalgae. J Biosci Bioeng. (2006) 101:87–96. 10.1263/jbb.101.8716569602
18. FAO. A Review on Culture, Production and Use of Spirulina as Food for Humans and Feeds for Domestic Animals and Fish. Rome: FAO Fisheries and Aquaculture Circular N° 1034 (2008).
19. Wolkers H, Barbosa M, Kleinegris DMM, Bosma R, Wijffels RH. Microalgae: the green gold of the future? In: Harmsen P, editor. Large-Scale Sustainable Cultivation of Microalgae for the Production of Bulk Commodities. Wageningen: Propress (2011) p. 1–34.
20. Van Krimpen M, Bikker P, Van der Meer I, Van der Peet-Schwering C, Vereijken J. Cultivation, Processing and Nutritional Aspects for Pigs and Poultry of European Protein Sources as Alternatives for Imported Soybean Products. Lelystad: Wageningen UR Livestock Research (2013).
21. de Vries M, de Boer IJM. Comparing environmental impacts for livestock products: a review of life cycle assessments. Livest Sci. (2010) 128:1–11. 10.1016/j.livsci.2009.11.007
22. Smetana S, Sandmann M, Rohn S, Pleissner D, Heinz V. Autotrophic and heterotrophic microalgae and cyanobacteria cultivation for food and feed: life cycle assessment. Bioresour Technol. (2017) 245:162–70. 10.1016/j.biortech.2017.08.11328892686
23. FAO. Review Paper, Algae-based Biofuels: Applications and Co-products. Rome: Food and Agriculture Organization of the United Nations (2010).
24. Becker EW. Micro-algae as a source of protein. Biotechnol Adv. (2007) 25:207–10. 10.1016/j.biotechadv.2006.11.00217196357
25. Chronakis IS, Madsen M. Algal proteins. Handbook of food proteins. In: Phillips GO, Williams PA, editors. Woodhead Publishing Series in Food Sciences, Technology and Nutrition. (2011). p. 353–94.
26. Misurcova L, Bunka F, Vavra Ambrozova J, Machu L, Samek D, Kracmar S. Amino acid composition of algal products and its contribution to RDI. Food Chem. (2014) 151:120–5. 10.1016/j.foodchem.2013.11.04024423510
27. Carbonell-Capella JM, Buniowska M, Barba FJ, Esteve MJ, Frigola A. Analytical methods for determining bioavailability and bioaccessibility of bioactive compounds from fruits and vegetables: a review. Compr Rev Food Sci Food Saf. (2014) 13:155–71. 10.1111/1541-4337.12049
28. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, et al. Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol. (2017) 29:949–82. 10.1007/s10811-016-0974-528458464
29. Raposo MFJ, Bernardo de Morais AMM, Costa de Morais RMS. Emergent sources of prebiotics: seaweeds and microalgae. Mar Drugs (2016) 14:E27. 10.3390/md14020027
30. Moreno JF, Corzo N, Montilla A, Villamiel M, Olano A. Current state and latest advances in the concept, production and functionality of prebiotic oligosaccharides. Curr Opin Food Sci. (2017) 13:50–5. 10.1016/j.cofs.2017.02.009
31. Jutur PP, Nesamma AA, Shaikh KM. Algae-derived marine oligosaccharides and their biological applications. Front Mar Sci. (2016) 3:83. 10.3389/fmars.2016.00083
32. Peltomaa E, Johnson MD, Taipale SJ. Marine cryptophytes are great sources of EPA and DHA. Mar Drugs (2018) 16:3–14. 10.3390/md1601000329278384
33. Garcia JL, de Vicente M, Galan B. Microalgae, old sustainable food and fashion nutraceuticals. Microb Biotechnol. (2017) 10:1017–24. 10.1111/1751-7915.1280028809450
34. Enzing C, Ploeg M, Barbosa M, Sijtsma L. Technical Report EUR 26255. In: Vigani M, Parisi C, Rodriguez-Cerezo E, editors. Microalgae-based Products for the Food and Feed Sector: An Outlook for Europe. Luxembourg: Publications Office of the European Union (2014).
35. Ruiz J, Olivieri G, de Vree J, Bosma R, Willems P, Reith JH, et al. Towards industrial products from microalgae. Energy Environ Sci. (2016) 9:3036–43. 10.1039/C6EE01493C
36. Brennan L, Owende P. Biofuels from microalgae–a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energy Rev. (2008) 14:557–77. 10.1016/j.rser.2009.10.009
37. Chacón-Lee TL, González-Mariño GE. Microalgae for “healthy” foods-possibilities and challenges. Compr Rev Food Sci Food Saf. (2010) 9:655–75. 10.1111/j.1541-4337.2010.00132.x
38. Fasaei F, Bitter JH, Slegers PM, van Boxtel AJB. Techno-economic evaluation of microalgae harvesting and dewatering systems. Algal Res. (2018) 31:347–62. 10.1016/j.algal.2017.11.038
39. EARTO. The TRL Scale as a Research & Innovation Policy Tool, EARTO Recommendations (2014).
40. 't Lam GP, Vermuë MH, Eppink MHM, Wijffels RH, van den Berg C. Multi-product microalgae biorefineries: from concept towards reality. Trends Biotechnol. (2018) 36:216–27. 10.1016/j.tibtech.2017.10.01129132753
41. Matos J, Cardoso C, Bandarra NM, Afonso C. Microalgae as healthy ingredients for functional food: a review. Food Func. (2017) 8:2672–85. 10.1039/C7FO00409E28681866
42. Mathys A, Georget E, Waldeck P, Petrusan J, Heinz V. Sustainable protein supply by algae biorefinery concepts. In: EFFoST Congress-Biobased Technologis in the Context of European Innovations Systems. Bologna (2013).
43. Sharma N, Sharma P. Industrial and biotechnological applications of algae: a review. J Adv Plant Biol. (2017) 1:1–26
44. Caporgno MP, Bengoa C. Anaerobic digestion of microalgae: the benefits of digesting microalgae waste. Curr Biochem Eng Special Issue Biomethane (2016) 3:210–22. 10.2174/1570180813666160527114809
45. Pittman JK, Dean AP, Osundeko O. The potential of sustainable algal biofuel production using wastewater resources. Bioresource Technol. (2011) 102:17–25. 10.1016/j.biortech.2010.06.03520594826
46. Christenson L, Sims R. Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv. (2011) 29:686–702. 10.1016/j.biotechadv.2011.05.01521664266
47. Carrasco-Castilla J, Hernández-Alvarez AJ, Jiménez-Martínez C, Gutiérrez-López GF, Dávila-Ortiz G. Use of proteomics and peptidomics methods in food bioactive peptide science and engineering. Food Eng Rev. (2012) 4:224–43. 10.1007/s12393-012-9058-8
48. Samarakoon K, Jeon YJ. Bio-functionalities of proteins derived from marine algae. Food Res Int. (2012) 48:948–60. 10.1016/j.foodres.2012.03.013
49. Kent M, Welladsen HM, Mangott A, Li Y. Nutritional evaluation of Australian microalgae as potential human health supplements. PLoS ONE (2015) 10:e0118985. 10.1371/journal.pone.011898525723496
50. Pihlanto-Leppäla A. Bioactive peptides derived from bovine whey proteins: opioid and ace-inhibitory peptides. Trends Food Sci Technol. (2000) 11:347–56. 10.1016/S0924-2244(01)00003-6
51. Korhonen H, Pihlanto A. Bioactive peptides: production and functionality. Int Dairy J. (2006) 16:945–60. 10.1016/j.idairyj.2005.10.012
52. Suetsuna K, Chen JR. Identification of antihypertensive peptides from peptic digest of two microalgae, Chlorella vulgaris and Spirulina platensis. Mar Biotechnol. (2001) 3:305–09. 10.1007/s10126-001-0012-714961345
53. Morris HJ, Carrillo O, Almarales A, Bermúdez RC, Alonso ME, Borges L, et al. Protein hydrolysates from the alga Chlorella vulgaris 87/1 with potentialities in immunonutrition. Biotecnol Aplicada (2009) 26:162–5. Available online at: http://scielo.sld.cu/scielo.php?script=sci_arttext&pid=S1027-28522009000200009
54. Sheih IC, Fang TJ, Wu TK. Isolation and characterisation of a novel angiotensin I-converting enzyme (ACE) inhibitory peptide from the algae protein waste. Food Chem. (2009) 115:279–84. 10.1016/j.foodchem.2008.12.019
55. Lauritano C, Andersen JH, Hansen E, Albrigtsen M, Escalera L, Esposito F, et al. Bioactivity screening of microalgae for antioxidant, anti-inflammatory, anticancer, anti-diabetes, and antibacterial activities. Front Mar Sci. (2016) 3:68. 10.3389/fmars.2016.00068
56. Admassu H, Abdalbasit M, Gasmalla A, Yang R, Zhao W. Bioactive peptides derived from seaweed protein and their health benefits: antihypertensive, antioxidant, and antidiabetic properties. J Food Sci. (2017) 83:6–16. 10.1111/1750-3841.1401129227526
57. Ngo DH, Vo TS, Ngo DN, Wijesekara I, Kim SK. Biological activities and potential health benefits of bioactive peptides derived from marine organisms. Int J Biol Macromol. (2012) 51:378–83. 10.1016/j.ijbiomac.2012.06.00122683669
58. Schwenzfeier A, Wierenga PA, Gruppen H. Isolation and characterization of soluble protein from the green microalgae Tetraselmis sp. Bioresour Technol. (2011) 102:9121–7. 10.1016/j.biortech.2011.07.04621831634
59. Tang G, Suter PM. Vitamin A, nutrition, and health values of algae: Spirulina, Chlorella, and Dunaliella. J Pharm Nutr Sci. (2011) 1:111–8. 10.6000/1927-5951.2011.01.02.04
60. Fan X, Bai L, Zhu L, Yang L, Zhang X. Marine algae-derived bioactive peptides for human nutrition and health. J Agric Food Chem. (2014) 62:9211–22. 10.1021/jf502420h25179496
61. Choe E, Min DB. Mechanisms of antioxidants in the oxidation of foods. Compr Rev Food Sci Food Saf. (2009) 8:345–58. 10.1111/j.1541-4337.2009.00085.x
62. Carocho M, Barreiro MF, Morales P, Ferreira ICFR. Adding molecules to food, pros and cons: a review on synthetic and natural food additives. Compr Rev Food Sci Food Saf. (2014) 13:377–99. 10.1111/1541-4337.12065
63. Asioli D, Aschemann-Witzel J, Caputo V, Vecchio R, Annunziata A, Næs T, et al. Making sense of the “clean label” trends: a review of consumer food choice behaviour and discussion of industry implications. Food Res Int. (2017) 99:58–71. 10.1016/j.foodres.2017.07.022
64. Raymundo A, Gouveia L, Batista AP, Empis J, Sousa I. Fat mimetic capacity of Chlorella vulgaris biomass in oil-in-water food emulsions stabilised by pea protein. Food Res Int. (2005) 38:961–65. 10.1016/j.foodres.2005.02.016
65. Gouveia L, Raymundo A, Batista AP, Sousa I, Empis J. Chlorella vulgaris and Haematococcus pluvialis biomass as colouring and antioxidant in food emulsions. Eur Food Res Technol. (2006) 222:362–7. 10.1007/s00217-005-0105-z
66. Batista AP, Gouveia L, Nunes MC, Franco JM, Raymundo A. Microalgae biomass as a novel functional ingredient in mixed gel systems. In: Williams PA, Phillips GO, editors. Gums and Stabilisers for the Food Industry, 14. Cambridge: RSC Publishing (2008).
67. Gouveia L, Batista AP, Raymundo A, Bandarra N. Spirulina maxima and Diacronema vlkianum microalgae in vegetable gelled desserts. J Nutr Food Sci. (2008) 38:492–501. 10.1108/00346650810907010
68. Batista AP, Nunes MC, Raymundo A, Gouveia L, Sousa I, Cordobés F, et al. Microalgae biomass interaction in biopolymer gelled systems. Food Hydrocolloids (2011) 25:817–825. 10.1016/j.foodhyd.2010.09.018
69. Batista AP, Nunes MC, Fradinho P, Gouveia L, Sousa I, Raymundo A, et al. Novel foods with microalgal ingredients—effect of gel setting conditions on the linear viscoelasticity of Spirulina and Haematococcus gels. J Food Eng. (2012) 110:182–9. 10.1016/j.jfoodeng.2011.05.044
70. Beheshtipour H, Mortazavian AM, Mohammadi R, Sohrabvandi S, Khosravi-Darani K. Supplementation of Spirulina platensis and Chlorella vulgaris algae into probiotic fermented milks. Compr Rev Food Sci Food Saf. (2013) 12:144–54. 10.1111/1541-4337.12004
71. Varga L, Szigeti J, Kovacs R, Foldes T, Buti S. Influence of a Spirulina platensis biomass on the microflora of fermented ABT milks during storage. J Dairy Sci. (2002) 85:1031–8. 10.3168/jds.S0022-0302(02)74163-512086036
72. Molnár N, Gyenis B, Varga L. Influence of a powdered Spirulina platensis biomass on acid production of lactococci in milk. Milchwissenschaft (2005) 60:380–382.
73. Parada JL, Zulpa de Caire G, Zaccaro de Mulé MC, Storni de Cano MM. Lactic acid bacteria growth promoters from Spirulina platensis. Int J Food Microbiol. (1998) 45:225–8. 10.1016/S0168-1605(98)00151-29927000
74. Cho EJ, Nam ES, Park SI. Keeping quality and sensory properties of drinkable yoghurt with added Chlorella extract. Korean J Food Nutr. (2004) 17:128–32. Available online at: http://www.koreascience.or.kr/article/ArticleFullRecord.jsp?cn=HGSPB1_2004_v17n2_128
75. Jeon JK. Effect of Chlorella addition on the quality of processed cheese. J Korean Soc Food Sci Nutr. (2006) 35:373–7. 10.3746/jkfn.2006.35.3.373
76. Gouveia L, Batista AP, Miranda A, Empis J, Raymundo A. Chlorella vulgaris biomass used as coloring source in traditional butter cookies. Innovative Food Sci Emerg Technol. (2007) 8:433–6. 10.1016/j.ifset.2007.03.026
77. Gouveia L, Coutinho C, Mendonça E, Batista AP, Sousa I, Bandarra NM, et al. Functional biscuits with PUFA-ω3 from Isochrysis galbana. J Sci Food Agric. (2008) 88:891–6. 10.1002/jsfa.3166
78. Abd El Baky HH, El Baroty GS, Ibrahem EA. Functional characters evaluation of biscuits sublimated with pure phycocyanin isolated from Spirulina and Spirulina biomass. Nutr Hosp. (2015) 32:231–41. 10.3305/nh.2015.32.1.880426262722
79. Singh P, Singh R, Jha A, Rasane P, Gautam AK. Optimization of a process for high fibre and high protein biscuit. J Food Sci Technol. (2015) 52:1394–403. 10.1007/s13197-013-1139-z25745207
80. Batista AP, Niccolai A, Fradinho P, Fragoso S, Bursic I, Rodolfi L, et al. Microalgae biomass as an alternative ingredient in cookies: sensory, physical and chemical properties, antioxidant activity and in vitro digestibility. Algal Res. (2017) 26:161–71. 10.1016/j.algal.2017.07.017
81. Mofasser Hossain AKM, Brennan MA, Mason SL, Guo X, Zeng XA, Brennan CS. The effect of astaxanthin-rich microalgae “Haematococcus pluvialis” and wholemeal flours incorporation in improving the physical and functional properties of cookies. Foods (2017) 6:57–67. 10.3390/foods6080057
82. Finney KF, Pomeranz Y, Bruinsma BL. Use of algae Dunaliella as a protein supplement in bread. Cereal Chem. (1984) 61:402–6.
83. Saleh AM, El-Fouly MM, Shaheen AB, El-Malky W, Khorshid AM. Blue-green algae in bread manufacture. (Blaugruene Algen bei der Brotherstellung). Getreide Mehl und Brot. (1987) 41:19–22.
84. Achour HY, Doumandji A, Sadi S, Saadi S. Evaluation of nutritional and sensory properties of bread enriched with Spirulina. Ann Food Sci Technol. (2014) 15:270–5. Available online at: http://www.afst.valahia.ro/images/documente/2014/issue2/full/section1/s01_w08_full.pdf
85. Ak B, Avşaroglu E, Işik O, Özyurt G, Kafkas E, Etyemez M, et al. Nutritional and physicochemical characteristics of bread enriched with microalgae Spirulina platensis. Int J Eng Res Appl. (2016) 6:30–8. Available online at: http://www.ijera.com/papers/Vol6_issue12/Part-4/E612043038.pdf
86. Dinu M, Vlasceanu G, Dune A, Rotaru G. Researches concerning the growth of nutritive value of the bread products through the Spirulina adding. J Environ Prot Ecol. (2012) 13:660–5. Available online at: http://www.jepe-journal.info/vol-13-no-2
87. Garcia-Segovia P, Pagan-Moreno MJ, Lara IF, Martinez-Monzo J. Effect of microalgae incorporation on physicochemical and textural properties in wheat bread formulation. Food Sci Technol Int. (2017) 23:437–47. 10.1177/108201321770025928675970
88. Figueira FDS, Crizel TDM, Silva CR, Sallas-Mellado MDLMS. Elaboration of gluten-free bread enriched with the microalgae Spirulina platensis. Braz J Food Technol. (2011) 14:308–16. 10.4260/BJFT2011140400037
89. Lucas BF, de Morais MG, Duarte Santos T, Vieira Costa JA. Spirulina for snack enrichment: nutritional, physical and sensory evaluations. LWT Food Sci Technol. (2018) 90:270–6. 10.1016/j.lwt.2017.12.032
90. Fradique M, Batista A, Nunes M, Gouveia L, Bandarra N, Raymundo A. Incorporation of Chlorella vulgaris and Spirulina maxima biomass on pasta products. Part 1: preparation and evaluation. J Sci Food Agric. (2010) 90:1656–64. 10.1002/jsfa.399920564448
91. Fradique M, Batista AP, Nunes MC, Gouveia L, Bandarra NM, Raymundo A. Isochrysis galbana and Diacronema vlkianum biomass incorporation in pasta products as PUFA's source. LWT J Food Sci Technol (2013) 50:312–9. 10.1016/j.lwt.2012.05.006
92. Rodríguez De Marco E, Steffolani ME, Martínez CS, León AE. Effects of Spirulina biomass on the technological and nutritional quality of bread wheat pasta. LWT J Food Sci Technol. (2014) 58:102–8. 10.1016/j.lwt.2014.02.054
93. El-Baz FK, Abdo SM, Hussein AMS. Microalgae Dunaliella salina for use as food supplement to improve pasta quality. Int J Pharm Sci Rev Res. (2017) 46:45–51. Available online at: http://globalresearchonline.net/journalcontents/v46-2/10.pdf
94. Prakash DR, Kumari P. Preparation of low-fat and high-protein frozen yoghurt enriched with papaya pulp and Spirulina. Trends Biosci. (2011) 4:182–94. Available online at: https://citeweb.info/20111153509
95. Ursu AV, Marcati A, Sayd T, Sante-Lhoutellier V, Djelveh G, Michaud P. Extraction, fractionation and functional properties of proteins from the microalgae Chlorella vulgaris. Bioresour Technol. (2014) 157:134–9. 10.1016/j.biortech.2014.01.07124534795