Advertisement

Effects of Solid-State Fermentation and the Potential Use of Cassava By-products as Fermented Food

  • Eduardo Marin Morales
  • Martina Zajul
  • Michael Goldman
  • Holger Zorn
  • Dejanira F. Angelis
Original Paper
  • 41 Downloads

Abstract

By-products such as cassava bagasse and leaves are discarded though they contain high amounts of carbohydrates, proteins, fat and minerals. The application of solid-state fermentation (SSF) to substrates containing these by-products could improve the bioavailability of nutrients while reducing the amounts of anti-nutritive factors such as cyanide. To evaluate the possibility of using by-products from cassava some techniques, such as colorimetric methods, gas chromatography and high performance of liquid chromatography were applied to evaluate the total cyanide, carbohydrate contents, to characterize the fatty acid profiles, and estimate the essential amino acids after the fermentation process. After the SSF process, the cyanide content was significantly decreased. The profile of essential amino acids showed high concentrations of histidine, isoleucine, valine, methionine and phenylalanine. Some important unsaturated fatty acids were found, such as linoleic acid (18:29,12); α-linolenic acid (18:39,12,15); 11-eicosenoic acid (20:1) and 13,16-docosadienoic acid (22:2). The evaluation of the protein quality showed a significant increase in its bioavailability. The results support the conclusion that currently not used agricultural by-products could become sources of food that provide important quantities of essential nutrients.

Keywords

By-products wastage Lentinula edodes Essential amino acids Cyanide Unsaturated fatty acids Protein bioavailability 

Notes

Acknowledgements

This work was supported by grants Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Supplementary material

12649_2018_479_MOESM1_ESM.docx (36 kb)
Supplementary Table S1 (DOCX 36 KB)

References

  1. 1.
    Fiorda, F.A., Soares Júnior, M.S., da Silva, F.A., Souto, L.R.F., Grosmann, M.V.E.: Amaranth flour, cassava starch and cassava bagasse in the production of gluten-free pasta: Technological and sensory aspects. Int. J. Food Sci. Technol. 48, 1977–1984 (2013).  https://doi.org/10.1111/ijfs.12179 CrossRefGoogle Scholar
  2. 2.
    de Oliveira, M.M.: Enriquecimento Nutricional por Bioconversão de Resíduos Agroindustriais para Utilização na Alimentação Animal. (2007)Google Scholar
  3. 3.
    Soccol, C.R., Vandenberghe, L.P.S.: Overview of applied solid-state fermentation in Brazil. Biochem. Eng. J. 13, 205–218 (2003).  https://doi.org/10.1016/S1369-703X(02)00133-X CrossRefGoogle Scholar
  4. 4.
    Vilhalva, D.A.A., Júnior, M.S.S., de Moura, C.M.A., Caligari, M., Souza, T.A.C., da Silva, F.A.: Utilization of cassava peel flour for preparing loaf bread. Rev. Inst. Adolfo Lutz. 70, 514–521 (2011)Google Scholar
  5. 5.
    Jasko, A.C., de Andrade, J., de Campos, P.F., Padilha, L., de Pauli, R.B., Quast, L.B., Schnitzle, E., Demiate, I.M.: Caracterização Físico-Química De Bagaço De Mandioca in Natura E Após Tratamento Hidrolítico. Rev. Bras. Tecnol. Agroindustrial 5, 427–441 (2011).  https://doi.org/10.3895/S1981-36862011000100006S1 CrossRefGoogle Scholar
  6. 6.
    Pandey, A., Soccol, C.R., Mitchell, D.: New developments in solid state fermentation: I-bioprocesses and products. Process Biochem. 35, 1153–1169 (2000).  https://doi.org/10.1016/S0032-9592(00)00152-7 CrossRefGoogle Scholar
  7. 7.
    Aro, S.: Improvement in the nutritive quality of cassava and its by-products through microbial fermentation. Afr. J. Biotechnol. 7, 4789–4797 (2008).  https://doi.org/10.4314/ajb.v7i25.59672 CrossRefGoogle Scholar
  8. 8.
    Latif, S., Müller, J.: Potential of cassava leaves in human nutrition: a review. Trends Food Sci. Technol. 44, 147–158 (2015).  https://doi.org/10.1016/j.tifs.2015.04.006 CrossRefGoogle Scholar
  9. 9.
    Nassar, N.M.A., Marques, A.O.: Cassava leaves as a source of protein. J. Food Agric. Environ. 4, 187–188 (2006)Google Scholar
  10. 10.
    Sagrilo, E.: Produtividade de três cultivares de mandioca (Manihot esculenta Crantz) em diferentes épocas de colheita no segundo ciclo vegetativo. (2001)Google Scholar
  11. 11.
    Helbig, E., Buchweitz, M.R.D., Gigante, D.P.: Analysis of hydrogen cyanide and phytic acid contents in feeding supplements. Multimixture. Rev. Nutr. 21, 323–328 (2008).  https://doi.org/10.1590/S1415-52732008000300007 CrossRefGoogle Scholar
  12. 12.
    Tangka, J.K.: Analysis of the thermal energy requirements for the extraction of leaf protein concentrate from some green plants. Biosyst. Eng. 86, 473–479 (2003)CrossRefGoogle Scholar
  13. 13.
    Câmara, F.S., Madruga, M.S.: Cyanic acid, phytic acid, total tannin and aflatoxin contents of a Brazilian (Natal) multimistura preparation. Rev. Nutr. 14, 33–36 (2001)CrossRefGoogle Scholar
  14. 14.
    Pandey, A.: Solid-state fermentation. Biochem. Eng. J. 13, 1–5 (2003)CrossRefGoogle Scholar
  15. 15.
    Couto, S.R., Sanromán, M.: Application of solid-state fermentation to food industry—a review. J. Food Eng. 76, 291–302 (2006).  https://doi.org/10.1016/j.jfoodeng.2005.05.022 CrossRefGoogle Scholar
  16. 16.
    Jin, B., Yan, X., Yu, Q., van Leeuwen, J.: A comprehensive pilot plant system for fungal biomass protein production and wastewater reclamation. Adv. Environ. Res. 6, 179–189 (2002).  https://doi.org/10.1016/S1093-0191(01)00049-1 CrossRefGoogle Scholar
  17. 17.
    Hölker, U., Lenz, J.: Solid-state fermentation—are there any biotechnological advantages? Curr. Opin. Microbiol. 8, 301–306 (2005).  https://doi.org/10.1016/j.mib.2005.04.006 CrossRefGoogle Scholar
  18. 18.
    Minotto, E., Bernardi, E., Donini, L.P., De Pelotas, U.F., : Mycelium growth in vitro of Pleurotus ostreatoroseus and colonization of the elephant grass substrate (Pennisetum purpureum Schum.) supplemented with different brans. Arq. do Instiuto Biológico 75, 379–383 (2008)Google Scholar
  19. 19.
    Schmidt, P., Wechsler, F.S., do Nascimento, J.S., Junior, F.M.D.: Pretreatment effects on fiber degradation of brachiaria hay by Pleurotus ostreatus fungus. Rev. Bras. Zootec. J. Anim. Sci. 32, 1866–1871 (2003).  https://doi.org/10.1590/S1516-35982003000800009 CrossRefGoogle Scholar
  20. 20.
    Gaitán-Hernández, R., Esqueda, M., Gutiérrez, A., Sánchez, A., Beltrán-García, M., Mata, G.: Bioconversion of agrowastes by Lentinula edodes: the high potential of viticulture residues. Appl. Microbiol. Biotechnol. 71, 432–439 (2006).  https://doi.org/10.1007/s00253-005-0241-1 CrossRefGoogle Scholar
  21. 21.
    Royse, D.J.: Cultivation of Shiitake on Natural and Synthetic Logs. The Pennsylvania State University, University Park (2009)Google Scholar
  22. 22.
    Kitzberger, C.S.G., Smânia, A., Pedrosa, R.C., Ferreira, S.R.S.: Antioxidant and antimicrobial activities of shiitake (Lentinula edodes) extracts obtained by organic solvents and supercritical fluids. J. Food Eng. 80, 631–638 (2007).  https://doi.org/10.1016/j.jfoodeng.2006.06.013 CrossRefGoogle Scholar
  23. 23.
    Bisen, P.S., Baghel, R.K., Sanodiya, B.S., Thakur, G.S., Prasad, G.B.K.S.: Lentinus edodes: a macrofungus with pharmacological activities. Curr. Med. Chem. 17, 2419–2430 (2010).  https://doi.org/10.2174/092986710791698495 CrossRefGoogle Scholar
  24. 24.
    Cunniff, P.: AOAC Official Methods of Analysis. AOAC, Arlington (1995)Google Scholar
  25. 25.
    Simonne, A.H., Simonne, E.H., Eitenmiller, R.R., Mills, H.A., Cresman, C.P.: Could the Dumas method replace the Kjeldahl digestion for nitrogen and crude protein determinations in foods? J. Sci. Food Agric. 73, 39–45 (1997).  https://doi.org/10.1002/(SICI)1097-0010(199701)73:1%3C39::AID-JSFA717%3E3.0.CO;2-4 CrossRefGoogle Scholar
  26. 26.
    Akeson, W.R., Stahmann, M.A.: A pepsin pancreatin digest index of protein quality evaluation. J. Nutr. 83, 257–261 (1964)CrossRefGoogle Scholar
  27. 27.
    Chaplin, M.F., Kennedy, J.F.: Carbohydrate Analysis: A Practical Approach. IRL Press Ltd., Oxford (1994)Google Scholar
  28. 28.
    Brito, V.H.S., Ramalho, R.T., Rabacow, A.P.M., Moreno, S.E., Cereda, M.: Colorimetric method for free and potential cyanide analysis of cassava tissue. Gene Conserv 8, 841–852 (2009)Google Scholar
  29. 29.
    Matthäus, B., Brühl, L.: Comparison of different methods for the determination of moisture content in biomass. J. Am. Oil Chem. Soc. 78, 95–102 (2001).  https://doi.org/10.1016/j.biombioe.2006.06.004 CrossRefGoogle Scholar
  30. 30.
    Ramani, B., Zorn, H., Papenbrock, J.: Quantification and fatty acid profiles of sulfolipids in two halophytes and a glycophyte grown under different salt concentrations. Z. Naturforsch. C 59, 835–842 (2004)CrossRefGoogle Scholar
  31. 31.
    Moore, S., Spackman, D.H., Stein, W.H.: Chromatography of amino acids on sulfonated polystyrene resins. Anal. Chem. 30, 1185–1190 (1958)CrossRefGoogle Scholar
  32. 32.
    Arreguín-Espinosa, R., Arreguín, B., González, C.: Purification and properties of a lipase from Cephaloleia presignis (Coleoptera, chrysomelidae). Biotechnol. Appl. Biochem. 31(Pt 3), 239–244 (2000)CrossRefGoogle Scholar
  33. 33.
    Stephan, A., Ahlborn, J., Zajul, M., Zorn, H.: Edible mushroom mycelia of Pleurotus sapidus as novel protein sources in a vegan boiled sausage analog system: functionality and sensory tests in comparison to commercial proteins and meat sausages. Eur. Food Res. Technol. (2017).  https://doi.org/10.1007/s00217-017-3012-1 CrossRefGoogle Scholar
  34. 34.
    Gorbics, L., Urge, L., Otvos, L.: Comparative and optimized dabsyl-amino acid analysis of synthetic phosphopeptides and glycopeptides. J. Chromatogr. A. 676, 169–176 (1994).  https://doi.org/10.1016/0021-9673(94)80459-1 CrossRefGoogle Scholar
  35. 35.
    Simpson, R.J., Neuberger, M.R., Liu, T.-Y.: Complete amino acid analysis hydrolysate. J. Biol. Chem. 251, 1936–1940 (1976)Google Scholar
  36. 36.
    Tirapegui, J., Macedo, M.: Metabolismo de Proteínas. In: Fisiologia da Nutrição Humana. Aspectos Básicos, Aplicados e Funcionais. pp. 69–109 (2007)Google Scholar
  37. 37.
    FAO/WHO: Dietary Protein Quality Evaluation in Human Nutrition. Food and Agriculture Organization of the United Nations, Auckland (2013)Google Scholar
  38. 38.
    Ford, J.E.: A microbiological method for assessing the nutritional value of proteins. Br. J. Nutr. 14, 485–497 (1960)CrossRefGoogle Scholar
  39. 39.
    Tavano, O.L., da Silva Júnior, S.I., Demonte, A., Neves, V.A.: Nutritional evaluation of chickpea protein: microbiological and chemical methods. Aliment. E Nutr. 15, 17–22 (2004)Google Scholar
  40. 40.
    Krishna, C.: Solid-state fermentation systems—an overview. Crit. Rev. Biotechnol. 25, 1–30 (2005).  https://doi.org/10.1080/07388550590925383 CrossRefGoogle Scholar
  41. 41.
    Jecu, L.: Solid state fermentation of agricultural wastes for endoglucanase production. Ind. Crops Prod. 11, 1–5 (2000).  https://doi.org/10.1016/S0926-6690(99)00022-9 CrossRefGoogle Scholar
  42. 42.
    Fakas, S., Makri, A., Mavromati, M., Tselepi, M., Aggelis, G.: Fatty acid composition in lipid fractions lengthwise the mycelium of Mortierella isabellina and lipid production by solid state fermentation. Bioresour. Technol. 100, 6118–6120 (2009).  https://doi.org/10.1016/j.biortech.2009.06.015 CrossRefGoogle Scholar
  43. 43.
    Kornijezuk, N.B.S.: Segurança Alimentar e Nutricional: uma questão de direito (2008). http://bdtd.bce.unb.br/tedesimplificado/tde_busca/arquivo.php?codArquivo=4360. Accessed 04 Mar 2010
  44. 44.
    Bôas, S.G.V.: Conversão do bagaço de maçã por Candida utilis e Pleurotus ostreatus visando a produção de suplemento para ração animal. (2001)Google Scholar
  45. 45.
    Kemdirim, O.C., Chukwu, O.A., Achinewhu, S.C.: Effect of traditional processing of cassava on the cyanide content of gari and cassava flour. Plant Foods Hum. Nutr. 48, 335–339 (1995).  https://doi.org/10.1007/BF01088492 CrossRefGoogle Scholar
  46. 46.
    Kobawila, S.C., Louembe, D., Keleke, S., Hounhouigan, J., Gamba, C.: Reduction of the cyanide content during fermentation of cassava roots and leaves to produce bikedi and ntoba mbodi, two food products from Congo. Afr. J. Biotechnol. 4, 689–696 (2005)CrossRefGoogle Scholar
  47. 47.
    Simeonova, F., Fishbein, L.: Hydrogen Cyanide and Cyanides. Human Health Aspects., Geneva (2004)Google Scholar
  48. 48.
    Howlett, W.P., Brubaker, G.R., Mlingi, N., Rosling, H.: Konzo, an epidemic upper motor neuron disease studied in Tanzania. Brain 113, 223–235 (1990)CrossRefGoogle Scholar
  49. 49.
    Mlingi, N.L.V., Assey, V., Poulter, N.H., Rosling, H.: Cyanohydrins from insufficiently processed cassava induces “konzo”, a newly identified paralytic disease in man. In: Proceedings of a Regional Workshop on Traditonal African Foods: Quality and Nutrition. pp. 25–29, Dar-es-Salaam (1991)Google Scholar
  50. 50.
    Fasuyi, A.O.: Nutrient composition and processing effects on cassava leaf (Manihot esculenta, Crantz) antinutrients. Pak. J. Nutr. 4, 37–42 (2005).  https://doi.org/10.3923/pjn.2005.37.42 CrossRefGoogle Scholar
  51. 51.
    Mann, J., Truswell, S.: Essentials of Human Nutrition. Oxford University Press, Oxford (2012)Google Scholar
  52. 52.
    Figuerola, F., Hurtado, M.L., Estévez, A.M., Chiffelle, I., Asenjo, F.: Fibre concentrates from apple pomace and citrus peel as potential fibre sources for food enrichment. Food Chem. 91, 395–401 (2005).  https://doi.org/10.1016/j.foodchem.2004.04.036 CrossRefGoogle Scholar
  53. 53.
    German, J.B.: Dietary lipids from an evolutionary perspective: sources, structures and functions. Matern. Child Nutr. 7, 2–16 (2011).  https://doi.org/10.1111/j.1740-8709.2011.00300.x CrossRefGoogle Scholar
  54. 54.
    Rustan, A.C., Drevon, C.: Fatty Acids: Structures and Properties. Wiley: New York (2005)Google Scholar
  55. 55.
    Zielińska, A., Nowak, I.: Fatty acids in vegetable oils and their importance in cosmetic industry. Chemik 68, 103–110 (2014)Google Scholar
  56. 56.
    Vannice, G., Rasmussen, H.: Position of the academy of nutrition and dietetics: dietary fatty acids for healthy adults. J. Acad. Nutr. Diet. 114, 136–153 (2014).  https://doi.org/10.1016/j.jand.2013.11.001 CrossRefGoogle Scholar
  57. 57.
    Gressler, V., Yokoya, N.S., Fujii, M.T., Colepicolo, P., Filho, J.M., Torres, R.P., Pinto, E.: Lipid, fatty acid, protein, amino acid and ash contents in four Brazilian red algae species. Food Chem. 120, 585–590 (2010).  https://doi.org/10.1016/j.foodchem.2009.10.028 CrossRefGoogle Scholar
  58. 58.
    Whelan, J.: The health implications of changing linoleic acid intakes. Prostaglandins Leukot. Essent. Fatty Acids 79, 165–167 (2008).  https://doi.org/10.1016/j.plefa.2008.09.013 CrossRefGoogle Scholar
  59. 59.
    Farvid, M.S., Ding, M., Pan, A., Sun, Q., Chiuve, S.E., Steffen, L.M., Willett, W.C., Hu, F.B.: Dietary linoleic acid and risk of coronary heart disease: a systematic review and meta-analysis of prospective cohort studies. Circulation 130, 1568–1578 (2014).  https://doi.org/10.1161/CIRCULATIONAHA.114.010236 CrossRefGoogle Scholar
  60. 60.
    Ando, Y., Sasaki, T.: GC separation of cis-eicosenoic acid positional isomers on an ionic liquid SLB-IL100 stationary phase. JAOCS J. Am. Oil Chem. Soc. 88, 743–748 (2011).  https://doi.org/10.1007/s11746-010-1733-4 CrossRefGoogle Scholar
  61. 61.
    Henry, G.E., Momin, R.A., Nair, M.G., Dewitt, D.L.: Antioxidant and cyclooxygenase activities of fatty acids found in food. J. Agric. Food Chem. 50, 2231–2234 (2002).  https://doi.org/10.1021/jf0114381 CrossRefGoogle Scholar
  62. 62.
    Kikukawa, H., Sakuradani, E., Nishibaba, Y., Okuda, T., Ando, A., Shima, J., Shimizu, S., Ogawa, J.: Production of cis-11-eicosenoic acid by Mortierella fungi. J. Appl. Microbiol. 118, 641–647 (2015).  https://doi.org/10.1111/jam.12725 CrossRefGoogle Scholar
  63. 63.
    Pereira, D.M., Valentão, P., Teixeira, N., Andrade, P.B.: Amino acids, fatty acids and sterols profile of some marine organisms from Portuguese waters. Food Chem. 141, 2412–2417 (2013).  https://doi.org/10.1016/j.foodchem.2013.04.120 CrossRefGoogle Scholar
  64. 64.
    Adeyeye, E.I.: The effect of fermentation on the dietary quality of lipids from African locust bean (Parkia biglobosa) seeds bean (Parkia biglobosa) seeds. Elixir Food Sci. 58, 14912–14922 (2013)Google Scholar
  65. 65.
    Nasaruddin, M.L., Hölscher, C., Kehoe, P., Graham, S.F., Green, B.D.: Wide-ranging alterations in the brain fatty acid complement of subjects with late Alzheimer’s disease as detected by GC-MS. Am. J. Transl. Res. 8, 154–165 (2016)Google Scholar
  66. 66.
    Serafeimidou, A., Zlatanos, S., Kritikos, G., Tourianis, A.: Change of fatty acid profile, including conjugated linoleic acid (CLA) content, during refrigerated storage of yogurt made of cow and sheep milk. J. Food Compos. Anal. 31, 24–30 (2013).  https://doi.org/10.1016/j.jfca.2013.02.011 CrossRefGoogle Scholar
  67. 67.
    Mello, L.D., Pinheiro, M.F.: Aspectos físico-químicos de azeites de oliva e de folhas de oliveira provenientes de cultivares do RS, Brasil. Aliment. e Nutr. 23, 537–548 (2012)Google Scholar
  68. 68.
    Boland, M.J., Rae, A.N., Vereijken, J.M., Meuwissen, M.P.M., Fischer, A.R.H., van Boekel, M.A.J.S., Rutherfurd, S.M., Gruppen, H., Moughan, P.J., Hendriks, W.H.: The future supply of animal-derived protein for human consumption. Trends Food Sci. Technol. 29, 62–73 (2013).  https://doi.org/10.1016/j.tifs.2012.07.002 CrossRefGoogle Scholar
  69. 69.
    Donini, L.P., Bernardi, E., Minotto, E., Nascimento, J.S.: In vitro development of Pleurotus ssp. Under the effect of substrates and dextrose. Arq. do Instiuto Biológico 72, 331–338 (2005)Google Scholar
  70. 70.
    Alonso, R., Grant, G., Dewey, P., Marzo, F.: Nutritional assessment in vitro and in vivo of raw and extruded peas (Pisum sativum L.). J. Agric. Food Chem. 48, 2286–2290 (2000)CrossRefGoogle Scholar
  71. 71.
    Mattila, P., Salo-Väänänen, P., Könkö, K., Aro, H., Jalava, T.: Basic composition and amino acid contents of mushrooms cultivated in Finland. J. Agric. Food Chem. 50, 6419–6422 (2002).  https://doi.org/10.1021/jf020608m CrossRefGoogle Scholar
  72. 72.
    Wu, G.: Amino acids: metabolism, functions, and nutrition. Amino Acids 37, 1–17 (2009).  https://doi.org/10.1007/s00726-009-0269-0 CrossRefGoogle Scholar
  73. 73.
    Tacon, A.G.J., Metian, M.: Fish matters: importance of aquatic foods in human nutrition and global food supply. Rev. Fish. Sci. 21, 22–38 (2013).  https://doi.org/10.1080/10641262.2012.753405 CrossRefGoogle Scholar
  74. 74.
    FAO/WHO: Necessidades de energia y de proteínas. In: Informe de una reunión consultiva conjunta fao/who/unu de expertos. p. 220, Genebra (1985)Google Scholar
  75. 75.
    Wu, G.: Amino Acids: Biochemistry and Nutrition. Taylor & Francis Group. LLC, Boca Raton (2013)CrossRefGoogle Scholar
  76. 76.
    Ford, J.E.: A microbiological method for assessing the nutritional value of proteins. Br. J. Nutr. 16, 409–425 (1962)CrossRefGoogle Scholar
  77. 77.
    Hegsted, D.M., Neff, R., Worcester, J.: Determination of the relative nutritive value of proteins. J. Agric. Food Chem. 16, 190–195 (1968)CrossRefGoogle Scholar
  78. 78.
    Gupta, U.C., Gupta, S.C.: Sources and deficiency diseases of mineral nutrients in human health and nutrition: a review. Pedosphere 24, 13–38 (2014).  https://doi.org/10.1016/S1002-0160(13)60077-6 CrossRefGoogle Scholar
  79. 79.
    Soetan, K.O., Olaiya, C.O., Oyewole, O.E.: The importance of mineral elements for humans, domestic animals and plants: a review. Afr. J. Food Sci. 4, 200–222 (2010)Google Scholar
  80. 80.
    Monti, A., Di Virgilio, N., Venturi, G.: Mineral composition and ash content of six major energy crops. Biomass Bioenergy 32, 216–223 (2008).  https://doi.org/10.1016/j.biombioe.2007.09.012 CrossRefGoogle Scholar
  81. 81.
    Coelho, M.S., Salas-Mellado, M., de las, M.: Chemical Characterization of CHIA (Salvia hispanica L.) for use in food products. J. Food Nutr. Res. 2, 263–269 (2014).  https://doi.org/10.12691/jfnr-2-5-9 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Department of Biochemistry and Microbiology, Institute of BiosciencesUNESP—Universidade Estadual PaulistaRio ClaroBrazil
  2. 2.Institute of Chemistry and Biotechnology of FoodJustus Liebig University GiessenGiessenGermany

Personalised recommendations