Should research on the nutritional potential and health benefits of fermented cereals focus more on the general health status of populations in developing countries?

Microorganisms

Volumn 5, Issue 3, 2017, Pages

  Laurent Babot, Caroline ^a   Guyot, Jean Pierre ^a  

^a UNIV MONTPELLIER   (France)

Author keywords

Antioxidant; Infection; Inflammation; Lactic acid bacteria; Low income countries; Malnutrition; Oxidative stress

Indexed keywords

EID: 85055951207     PISSN: None     EISSN: 20762607     Source Type: Journal    
DOI: 10.3390/microorganisms5030040     Document Type: Article

References (73)

1. FAOSTAT. Available online: http://www.fao.org/faostat/en/#home (accessed on 2 June 2017).
2. Galati, A.; Oguntoyinbo, F.A.; Moschetti, G.; Crescimanno, M.; Settanni, L. The Cereal Market and the Role of Fermentation in Cereal-Based Food Production in Africa. Food Rev. Int. 2014, 30, 317–337. [CrossRef]
3. Arendt, E.K.; Moroni, A.; Zannini, E. Medical nutrition therapy: Use of sourdough lactic acid bacteria as a cell factory for delivering functional biomolecules and food ingredients in gluten free bread. Microb. Cell Fact. 2011, 10, S15. [CrossRef] [PubMed]
4. Cross, M.L.; Stevenson, L.M.; Gill, H.S. Anti-allergy properties of fermented foods: An important immunoregulatory mechanism of lactic acid bacteria? Int. Immunopharmacol. 2001, 1, 891–901. [CrossRef]
5. Marco, M.L.; Heeney, D.; Binda, S.; Cifelli, C.J.; Cotter, P.D.; Foligné, B.; Gänzle, M.; Kort, R.; Pasin, G.; Pihlanto, A.; et al. Health benefits of fermented foods: Microbiota and beyond. Curr. Opin. Biotechnol. 2017, 44, 94–102. [CrossRef] [PubMed]
6. Chavan, J.K.; Kadam, S.S.; Beuchat, L.R. Nutritional improvement of cereals by fermentation. Crit. Rev. Food Sci. Nutr. 1989, 28, 349–400. [CrossRef] [PubMed]
7. Calasso, M.; Vincentini, O.; Valitutti, F.; Felli, C.; Gobbetti, M.; Cagno, R.D. The sourdough fermentation may enhance the recovery from intestinal inflammation of coeliac patients at the early stage of the gluten-free diet. Eur. J. Nutr. 2012, 51, 507–512. [CrossRef] [PubMed]
8. Gänzle, M.G.; Loponen, J.; Gobbetti, M. Proteolysis in sourdough fermentations: Mechanisms and potential for improved bread quality. Trends Food Sci. Technol. 2008, 19, 513–521. [CrossRef]
9. De Angelis, M.; Coda, R.; Silano, M.; Minervini, F.; Rizzello, C.G.; Di Cagno, R.; Vicentini, O.; De Vincenzi, M.; Gobbetti, M. Fermentation by selected sourdough lactic acid bacteria to decrease coeliac intolerance to rye flour. J. Cereal Sci. 2006, 43, 301–314. [CrossRef]
10. Di Cagno, R.; Rizzello, C.G.; De Angelis, M.; Cassone, A.; Giuliani, G.; Benedusi, A.; Limitone, A.; Surico, R.F.; Gobbetti, M. Use of Selected Sourdough Strains of Lactobacillus for Removing Gluten and Enhancing the Nutritional Properties of Gluten-Free Bread. J. Food Prot. 2008, 71, 1491–1495. [CrossRef] [PubMed]
11. Guyot, J.-P. Cereal-based fermented foods in developing countries: Ancient foods for modern research. Int. J. Food Sci. Technol. 2012, 47, 1109–1114. [CrossRef]
12. De Vuyst, L.; Neysens, P. The sourdough microflora: Biodiversity and metabolic interactions. Trends Food Sci. Technol. 2005, 16, 43–56. [CrossRef]
13. De Vuyst, L.; Van Kerrebroeck, S.; Harth, H.; Huys, G.; Daniel, H.-M.; Weckx, S. Microbial ecology of sourdough fermentations: Diverse or uniform? Food Microbiol. 2014, 37, 11–29. [CrossRef] [PubMed]
14. Poutanen, K.; Flander, L.; Katina, K. Sourdough and cereal fermentation in a nutritional perspective. Food Microbiol. 2009, 26, 693–699. [CrossRef] [PubMed]
15. Now Available: The 2016 Global Nutrition Report. Available online: http://www.globalnutritionreport.org/2016/06/14/now-available-the-2016-global-nutrition-report/(accessed on 2 June 2017).
16. World Health Organization. Human Vitamin and Mineral Requirements: Report of a Joint FAO/WHO Expert Consultation, Bangkok, Thailand; World Health Organization: Geneva, Switzerland, 2002.
17. Greffeuille, V.; Polycarpe Kayodé, A.P.; Icard-Vernière, C.; Gnimadi, M.; Rochette, I.; Mouquet-Rivier, C. Changes in iron, zinc and chelating agents during traditional African processing of maize: Effect of iron contamination on bioaccessibility. Food Chem. 2011, 126, 1800–1807. [CrossRef] [PubMed]
18. Saubade, F.; Hemery, Y.M.; Guyot, J.-P.; Humblot, C. Lactic acid fermentation as a tool for increasing the folate content of foods. Crit. Rev. Food Sci. Nutr. 2016. [CrossRef] [PubMed]
19. Saubade, F.; Humblot, C.; Hemery, Y.M.; Guyot, J.-P. PCR screening of an African fermented pearl-millet porridge metagenome to investigate the nutritional potential of its microbiota. Int. J. Food Microbiol. 2017, 244, 103–110. [CrossRef] [PubMed]
20. Turpin, W.; Humblot, C.; Guyot, J.-P. Genetic screening of functional properties of lactic acid bacteria in a fermented pearl millet slurry and in the metagenome of fermented starchy foods. Appl. Environ. Microbiol. 2011. [CrossRef] [PubMed]
21. WHO|The African Regional Health Report: The Health of the People. Available online: http://www.who. int/bulletin/africanhealth/en/(accessed on 6 June 2017).
22. GHO|By Category|WORLD—Diarrhoeal Diseases. Available online: http://apps.who.int/gho/data/view. main.CM1002015WORLD-CH3 (accessed on 6 June 2017).
23. Overview|African Health Observatory. Available online: http://www.aho.afro.who.int/en/atlas/overview (accessed on 6 June 2017).
24. Mbuya, M.N.N.; Humphrey, J.H. Preventing environmental enteric dysfunction through improved water, sanitation and hygiene: An opportunity for stunting reduction in developing countries. Matern. Child. Nutr. 2016, 12, 106–120. [CrossRef] [PubMed]
25. Dostal, A.; Gagnon, M.; Chassard, C.; Zimmermann, M.B.; O’Mahony, L.; Lacroix, C. Salmonella Adhesion, Invasion and Cellular Immune Responses Are Differentially Affected by Iron Concentrations in a Combined In Vitro Gut Fermentation-Cell Model. PLoS ONE 2014, 9, e93549. [CrossRef] [PubMed]
26. Paganini, D.; Uyoga, M.A.; Zimmermann, M.B. Iron Fortification of Foods for Infants and Children in Low-Income Countries: Effects on the Gut Microbiome, Gut Inflammation, and Diarrhea. Nutrients 2016, 8, 494. [CrossRef] [PubMed]
27. Jaeggi, T.; Kortman, G.A.M.; Moretti, D.; Chassard, C.; Holding, P.; Dostal, A.; Boekhorst, J.; Timmerman, H.M.; Swinkels, D.W.; Tjalsma, H.; et al. Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants. Gut 2014. [CrossRef] [PubMed]
28. Gwamaka, M.; Kurtis, J.D.; Sorensen, B.E.; Holte, S.; Morrison, R.; Mutabingwa, T.K.; Fried, M.; Duffy, P.E. Iron Deficiency Protects Against Severe Plasmodium falciparum Malaria and Death in Young Children. Clin. Infect. Dis. 2012, 54, 1137–1144. [CrossRef] [PubMed]
29. Gier de, B.; Ponce, M.C.; Perignon, M.; Fiorentino, M.; Khov, K.; Chamnan, C.; de Boer, M.R.; Parker, M.E.; Burja, K.; Dijkhuizen, M.A.; et al. Micronutrient-Fortified Rice Can Increase Hookworm Infection Risk: A Cluster Randomized Trial. PLoS ONE 2016, 11, e0145351. [CrossRef] [PubMed]
30. Coda, R.; Rizzello, C.G.; Gobbetti, M. Use of sourdough fermentation and pseudo-cereals and leguminous flours for the making of a functional bread enriched of γ-aminobutyric acid (GABA). Int. J. Food Microbiol. 2010, 137, 236–245. [CrossRef] [PubMed]
31. O’Mahony, L.; Feeney, M.; O’Halloran, S.; Murphy, L.; Kiely, B.; Fitzgibbon, J.; Lee, G.; O’Sullivan, G.; Shanahan, F.; Collins, J.K. Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice. Aliment. Pharmacol. Ther. 2001, 15, 1219–1225. [CrossRef] [PubMed]
32. Osman, N.; Adawi, D.; Ahrne, S.; Jeppsson, B.; Molin, G. Modulation of the Effect of Dextran Sulfate Sodium-Induced Acute Colitis by the Administration of Different Probiotic Strains of Lactobacillus and Bifidobacterium. Dig. Dis. Sci. 2004, 49, 320–327. [CrossRef] [PubMed]
33. Carroll, I.M.; Andrus, J.M.; Bruno-Bárcena, J.M.; Klaenhammer, T.R.; Hassan, H.M.; Threadgill, D.S. Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293, G729–G738. [CrossRef] [PubMed]
34. Lutgendorff, F.; Trulsson, L.M.; van Minnen, L.P.; Rijkers, G.T.; Timmerman, H.M.; Franzén, L.E.; Gooszen, H.G.; Akkermans, L.M.A.; Söderholm, J.D.; Sandström, P.A. Probiotics enhance pancreatic glutathione biosynthesis and reduce oxidative stress in experimental acute pancreatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 295, G1111–G1121. [CrossRef] [PubMed]
35. Lutgendorff, F.; Nijmeijer, R.M.; Sandström, P.A.; Trulsson, L.M.; Magnusson, K.-E.; Timmerman, H.M.; van Minnen, L.P.; Rijkers, G.T.; Gooszen, H.G.; Akkermans, L.M.A.; et al. Probiotics Prevent Intestinal Barrier Dysfunction in Acute Pancreatitis in Rats via Induction of Ileal Mucosal Glutathione Biosynthesis. PLoS ONE 2009, 4, e4512. [CrossRef] [PubMed]
36. Peran, L.; Camuesco, D.; Comalada, M.; Nieto, A.; Concha, A.; Adrio, J.L.; Olivares, M.; Xaus, J.; Zarzuelo, A.; Galvez, J. Lactobacillus fermentum, a probiotic capable to release glutathione, prevents colonic inflammation in the TNBS model of rat colitis. Int. J. Colorectal Dis. 2006, 21, 737–746. [CrossRef] [PubMed]
37. Oguntoyinbo, F.A.; Narbad, A. Multifunctional properties of Lactobacillus plantarum strains isolated from fermented cereal foods. J. Funct. Foods 2015, 17, 621–631. [CrossRef]
38. Reimund, J.-M. Stress oxydant au cours des syndromes inflammatoires chroniques. Nutr. Clin. Métab. 2002, 16, 275–284. [CrossRef]
39. Zazzo, J.-F. Stress oxydant au cours des états inflammatoires aigus et des états d’agression: Implications pour la pratique clinique. Nutr. Clin. Métab. 2002, 16, 268–274. [CrossRef]
40. Pasquier, C. Stress oxydatif et inflammation. Rev. Fr. Lab. 1995, 1995, 87–92. [CrossRef]
41. Hur, S.J.; Lee, S.Y.; Kim, Y.-C.; Choi, I.; Kim, G.-B. Effect of fermentation on the antioxidant activity in plant-based foods. Food Chem. 2014, 160, 346–356. [CrossRef] [PubMed]
42. Kim, H.S.; Chae, H.S.; Jeong, S.G.; Ham, J.S.; Im, S.K.; Ahn, C.N.; Lee, J.M. Antioxidant Activity of Some Yogurt Starter Cultures. Asian-Australas. J. Anim. Sci. Asian-Australas. J. Anim. Sci. 2005, 18, 255–258. [CrossRef]
43. Wang, Y.-C.; Yu, R.-C.; Chou, C.-C. Antioxidative activities of soymilk fermented with lactic acid bacteria and bifidobacteria. Food Microbiol. 2006, 23, 128–135. [CrossRef] [PubMed]
44. Hubert, J.; Berger, M.; Nepveu, F.; Paul, F.; Daydé, J. Effects of fermentation on the phytochemical composition and antioxidant properties of soy germ. Food Chem. 2008, 109, 709–721. [CrossRef] [PubMed]
45. Juan, M.-Y.; Chou, C.-C. Enhancement of antioxidant activity, total phenolic and flavonoid content of black soybeans by solid state fermentation with Bacillus subtilis BCRC 14715. Food Microbiol. 2010, 27, 586–591. [CrossRef] [PubMed]
46. Lin, M.-Y.; Yen, C.-L. Antioxidative Ability of Lactic Acid Bacteria. J. Agric. Food Chem. 1999, 47, 1460–1466. [CrossRef] [PubMed]
47. Spyropoulos, B.G.; Misiakos, E.P.; Fotiadis, C.; Stoidis, C.N. Antioxidant Properties of Probiotics and Their Protective Effects in the Pathogenesis of Radiation-Induced Enteritis and Colitis. Dig. Dis. Sci. 2011, 56, 285–294. [CrossRef] [PubMed]
48. Kullisaar, T.; Zilmer, M.; Mikelsaar, M.; Vihalemm, T.; Annuk, H.; Kairane, C.; Kilk, A. Two antioxidative lactobacilli strains as promising probiotics. Int. J. Food Microbiol. 2002, 72, 215–224. [CrossRef]
49. Chang, S.K.; Hassan, H.M. Characterization of superoxide dismutase in Streptococcus thermophilus. Appl. Environ. Microbiol. 1997, 63, 3732–3735. [PubMed]
50. Han, W.; Mercenier, A.; Ait-Belgnaoui, A.; Pavan, S.; Lamine, F.; van Swam, I.I.; Kleerebezem, M.; Salvador-Cartier, C.; Hisbergues, M.; Bueno, L.; et al. Improvement of an experimental colitis in rats by lactic acid bacteria producing superoxide dismutase. Inflamm. Bowel Dis. 2006, 12, 1044–1052. [CrossRef] [PubMed]
51. Kodali, V.P.; Sen, R. Antioxidant and free radical scavenging activities of an exopolysaccharide from a probiotic bacterium. Biotechnol. J. 2008, 3, 245–251. [CrossRef] [PubMed]
52. Othman, N.B.; Roblain, D.; Chammen, N.; Thonart, P.; Hamdi, M. Antioxidant phenolic compounds loss during the fermentation of Chétoui olives. Food Chem. 2009, 116, 662–669. [CrossRef]
53. Hole, A.S.; Rud, I.; Grimmer, S.; Sigl, S.; Narvhus, J.; Sahlstrøm, S. Improved Bioavailability of Dietary Phenolic Acids in Whole Grain Barley and Oat Groat following Fermentation with Probiotic Lactobacillus acidophilus, Lactobacillus johnsonii, and Lactobacillus reuteri. J. Agric. Food Chem. 2012, 60, 6369–6375. [CrossRef] [PubMed]
54. Dueñas, M.; Fernández, D.; Hernández, T.; Estrella, I.; Muñoz, R. Bioactive phenolic compounds of cowpeas (Vigna sinensis L.). Modifications by fermentation with natural microflora and with Lactobacillus plantarum ATCC 14917. J. Sci. Food Agric. 2005, 85, 297–304. [CrossRef]
55. Rodríguez, H.; Curiel, J.A.; Landete, J.M.; de las Rivas, B.; de Felipe, F.L.; Gómez-Cordovés, C.; Mancheño, J.M.; Muñoz, R. Food phenolics and lactic acid bacteria. Int. J. Food Microbiol. 2009, 132, 79–90. [CrossRef] [PubMed]
56. Đorđević, T.M.; Šiler-Marinković, S.S.; Dimitrijević-Branković, S.I. Effect of fermentation on antioxidant properties of some cereals and pseudo cereals. Food Chem. 2010, 119, 957–963. [CrossRef]
57. Madhujith, T.; Shahidi, F. Optimization of the Extraction of Antioxidative Constituents of Six Barley Cultivars and Their Antioxidant Properties. J. Agric. Food Chem. 2006, 54, 8048–8057. [CrossRef] [PubMed]
58. Sun, T.; Ho, C.-T. Antioxidant activities of buckwheat extracts. Food Chem. 2005, 90, 743–749. [CrossRef]
59. Liukkonen, K.-H.; Katina, K.; Wilhelmsson, A.; Myllymaki, O.; Lampi, A.-M.; Kariluoto, S.; Piironen, V.; Heinonen, S.-M.; Nurmi, T.; Adlercreutz, H.; et al. Process-induced changes on bioactive compounds in whole grain rye. Proc. Nutr. Soc. 2003, 62, 117–122. [CrossRef] [PubMed]
60. Chung, Y.-C.; Chang, C.-T.; Chao, W.-W.; Lin, C.-F.; Chou, S.-T. Antioxidative Activity and Safety of the 50 Ethanolic Extract from Red Bean Fermented by Bacillus subtilis IMR-NK1. J. Agric. Food Chem. 2002, 50, 2454–2458. [CrossRef] [PubMed]
61. Wang, C.-Y.; Wu, S.-J.; Shyu, Y.-T. Antioxidant properties of certain cereals as affected by food-grade bacteria fermentation. J. Biosci. Bioeng. 2014, 117, 449–456. [CrossRef] [PubMed]
62. Korhonen, H.; Pihlanto, A. Food-derived Bioactive Peptides—Opportunities for Designing Future Foods. Curr. Pharm. Des. 2003, 9, 1297–1308. [CrossRef] [PubMed]
63. Martínez-Augustin, O.; Rivero-Gutiérrez, B.; Mascaraque, C.; Sánchez de Medina, F. Food Derived Bioactive Peptides and Intestinal Barrier Function. Int. J. Mol. Sci. 2014, 15, 22857–22873. [CrossRef] [PubMed]
64. Malaguti, M.; Dinelli, G.; Leoncini, E.; Bregola, V.; Bosi, S.; Cicero, A.F.G.; Hrelia, S. Bioactive Peptides in Cereals and Legumes: Agronomical, Biochemical and Clinical Aspects. Int. J. Mol. Sci. 2014, 15, 21120–21135. [CrossRef] [PubMed]
65. Ortiz-Martinez, M.; Winkler, R.; García-Lara, S. Preventive and therapeutic potential of peptides from cereals against cancer. J. Proteom. 2014, 111, 165–183. [CrossRef] [PubMed]
66. Rizzello, C.G.; Nionelli, L.; Coda, R.; Gobbetti, M. Synthesis of the Cancer Preventive Peptide Lunasin by Lactic Acid Bacteria During Sourdough Fermentation. Nutr. Cancer 2012, 64, 111–120. [CrossRef] [PubMed]
67. Hernandez-Ledesma, B.; Hsieh, C.C.; de Lumen, O.B. Chemopreventive Properties of Peptide Lunasin: A Review. Protein Pept. Lett. 2013, 20, 424–432. [CrossRef] [PubMed]
68. Wong, C.G.T.; Bottiglieri, T.; Snead, O.C., III. GABA, γ-hydroxybutyric acid, and neurological disease. Ann. Neurol. 2003, 54, S3–S12. [CrossRef] [PubMed]
69. Lyte, M. Probiotics function mechanistically as delivery vehicles for neuroactive compounds: Microbial endocrinology in the design and use of probiotics. BioEssays 2011, 33, 574–581. [CrossRef] [PubMed]
70. Kook, M.-C.; Seo, M.-J.; Cheigh, C.-I.; Pyun, Y.-R.; Cho, S.-C.; Park, H. Enhanced production of gamma-aminobutyric acid using rice bran extracts by Lactobacillus sakei B2-16. J. Microbiol. Biotechnol. 2010, 20, 763–766. [PubMed]
71. Rizzello, C.G.; Cassone, A.; Di Cagno, R.; Gobbetti, M. Synthesis of Angiotensin I-Converting Enzyme (ACE)-Inhibitory Peptides and γ-Aminobutyric Acid (GABA) during Sourdough Fermentation by Selected Lactic Acid Bacteria. J. Agric. Food Chem. 2008, 56, 6936–6943. [CrossRef] [PubMed]
72. Koyama, M.; Naramoto, K.; Nakajima, T.; Aoyama, T.; Watanabe, M.; Nakamura, K. Purification and Identification of Antihypertensive Peptides from Fermented Buckwheat Sprouts. J. Agric. Food Chem. 2013, 61, 3013–3021. [CrossRef] [PubMed]
73. Coda, R.; Rizzello, C.G.; Pinto, D.; Gobbetti, M. Selected Lactic Acid Bacteria Synthesize Antioxidant Peptides during Sourdough Fermentation of Cereal Flours. Appl. Environ. Microbiol. 2012, 78, 1087–1096. [CrossRef] [PubMed]