Almond milk fermented with different potentially probiotic bacteria improves iron uptake by intestinal epithelial (Caco-2) cells

Neus  Bernat; Maite Chafer; Amparo  Chiralt; Jose Moises Laparra; Chelo Gonzalez-Martıne

doi:10.7455/ijfs/4.1.2015.a4

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Almond milk fermented with different potentially probiotic bacteria improves iron uptake by intestinal epithelial (Caco-2) cells

Published: 18.04.2015.

Volume 4, Issue 1 (2015)

pp. 49-60;

https://doi.org/10.7455/ijfs/4.1.2015.a4

Abstract

New fermented almond milks were developed, using different potentially probiotic bacteria, in order to meet the current demand for healthy, versatile non-dairy products. An in vitro digestion/Caco2 cell model was used to evaluate the effect of both non-fermented and fermented almond milks on the mitochondrial enzymatic activities of enterocytes. Moreover, macrophages were challenged with the in-vitro digested samples and the production of pro-inflammatory biomarkers TNF-α and IL-6 was quantified. Enzymatic activities of cell cultures seemed to be stimulated by the exposure to both fermented and non-fermented almond milks. Both biomarkers decreased (p< 0.05) in fermented almond milks with either B. bifidum or B. longum. Results showed that fermented almond products favored the energetic metabolism of enterocytes and had a lower inflammatory response than non-fermented almond milk, suggesting its benefits for the management of allergies/intolerances. Moreover, the fermentation process enhanced the uptake of iron by Caco-2 cells, especially when using L. rhamnosus and either B. bifidum or B. longum as starters, thus improving the product bioactivity. Therefore, new nondairy fermented products with functional properties were developed, which might be positioned as alternatives to cow-milk products for sensitized groups of population (allergic and/or intolerant to cow milk or anemic population, among others).

Keywords

References

Proulx A, Reddy M. Fermentation and lactic acid addition enhance iron bioavailability of maize. Journal of Agri-cultural and Food Chemistry. 2007;(7):2749–54.

Laparra J, Barbera R, Alegria A, Glahn R, Miller D. Purified glycosaminoglycans from cooked haddock may enhance fe uptake via endocytosis in a caco-2 cell culture model. Journal of Food Science. 2009;(6):168-H173.

Laparra J, Olivares M, Gallina O, Sanz Y. Bifidobacterium longum cect 7347 modulates immune responses in a gliadin-induced enteropathy animal model. Plos One. 2012;(2).

Laparra J, Tako E, Glahn R, Miller D. Inulin affects iron dialyzability from feso4 and feedta solutions but does not alter fe uptake by caco-2 cells. Journal of Agricultural and Food Chemistry. 2008;(8):2846–51.

Luengo M. La almendra y otros frutos secos: castaña, pistacho, piñon, nuez. 2009;

Lujan Capra M, Patrignani F, Del Lujan Quiberoni A, Alberto Reinheimer J, Lanciotti R, Guerzoni M. Effect of high pressure homogenization on lactic acid bacteria phages and probiotic bacteria phages. International Dairy Journal. 2009;(5):336–41.

Ma T, Iwamoto G, Hoa N, Akotia V, Pedram A, Boivin M, et al. Tnf-alphainduced increase in intestinal epithelial tight junction permeability requires nf-kappa b activation. American Journal of Physiology-gastrointestinal and Liver Physiology. 2004;(3):367-G376.

Mandalari G, Nueno-Palop C, Bisignano G, Wickham M, Narbad A. Potential prebiotic properties of almond (amygdalus communis l.) seeds. Applied and Environmental Microbiology. 2008;(14):4264–70.

Miret S, Simpson R, Mckie A. Physiology and molecular biology of dietary iron absorption. Annual Review of Nutrition. 2003;283–301.

10.

Novak T, Babcock T, Jho D, Helton W, Espat N. Nf-kappa b inhibition by omega-3 fatty acids modulates lps-stimulated macrophage tnf-alpha transcription. American Journal of Physiologylung Cellular and Molecular Physiology. 2003;(1):84-L89.

11.

Laparra J, Sanz Y. Bifidobacteria inhibit the inflammatory response induced by gliadins in intestinal epithelial cells via modifications of toxic peptide generation during digestion. Journal of Cellular Biochemistry. 2010;(4):801–7.

12.

Rajaram S, Connell K, Sabate J. Effect of almond-enriched highmonounsaturated fat diet on selected markers of inflammation: a randomised, controlled, crossover study. British Journal of Nutrition. 2010;(6):907–12.

13.

Sabaté J, Haddad E, Tanzman J, Jambazian P, Rajaram S. Serum lipid response to the graduated enrichment of a step i diet with almonds: a randomized feeding trial. American Journal of Clinical Nutrition. 2003;(6):1379–84.

14.

Scott K, Martin J, Duncan S, Flint H. Prebiotic stimulation of human colonic butyrate-producing bacteria and bifidobacteria, in vitro. Fems Microbiology Ecology. 2014;(1):30–40.

15.

Sutas Y, Soppi E, Korhonen H, Syvaoja E, Saxelin M, Rokka T, et al. Suppression of lymphocyte proliferation in vitro by bovine caseins hydrolyzed with lactobacillus casei gg-derived enzymes. Journal of Allergy and Clinical Immunology. 1996;(1):70245–7.

16.

Wagar L, Champagne C, Buckley N, Raymond Y, Green-Johnson J. Immunomodulatory properties of fermented soy and dairy milks prepared with lactic acid bacteria. Journal of Food Science. 2009;(8):423-M430.

17.

Wijeratne S, Abou-Zaid M, Shahidi F. Antioxidant polyphenols in almond and its coproducts. Journal of Agricultural and Food Chemistry. 2006;(2):312–8.

18.

Wu SB, Su JJ, Sun LH, Wang WX, Zhao Y, Li H, et al. Triterpenoids and steroids from the fruits of melia toosendan and their cytotoxic effects on two human cancer cell lines. Journal of Natural Products. 2010;(11):1898–906.

19.

Yada S, Lapsley K, Huang G. A review of composition studies of cul-tivated almonds: macronutrients and micronutrients. Journal of Food Composition and Analysis. 2011;(4–5):469–80.

20.

Deepika G, Rastall R, Charalampopoulos D. Effect of food models and low-temperature storage on the adhesion of lactobacillus rhamnosus gg to caco-2 cells. Journal of Agricultural and Food Chemistry. 2011;(16):8661–6.

21.

Cruz A, C. Caracterización y potencial probiótico de bacterias lácticas aisladas de leche de oveja guirra (Doctoral dissertation. 2011;

22.

Anandan C, Nurmatov U, Van Schayck O, Sheikh A. Is the prevalence of asthma declining? systematic review of epidemiological studies. Allergy. 2010;(2):152–67.

23.

Annunziata A, Vecchio R. Functional foods development in the european market: a consumer perspective. Journal of Functional Foods. 2011;(3):223–8.

24.

Artazcoz M, -O. Lactancia artificial: técnica, indicaciones, fórmulas especiales. Pediatría Integral. 2007;(4):318–26.

25.

Baroja M, Kirjavainen P, Hekmat S, Reid G. Anti-inflammatory effects of probiotic yogurt in inflammatory bowel disease patients. Clinical and Experimental Immunology. 2007;(3):470–9.

26.

Bergqvist S, Andlid T, Sandberg AS. Lactic acid fermentation stimulated iron absorption by caco-2 cells is associated with increased soluble iron content in carrot juice. British Journal of Nutrition. 2006;(4):705–11.

27.

Björkstén B. Current Opinion in Allergy and Clinical Immunology. 2009;(3):185–9.

28.

Chen CY, Lapsley K, Blumberg J. A nutrition and health perspective on almonds. Journal of the Science of Food and Agriculture. 2006;(14):2245–50.

29.

Cruz N, Capellas M, Jaramillo D, Trujillo A, Guamis B, Ferragut V. Soymilk treated by ultra highpressure homogenization: acid coagulation properties and characteristics of a soyyogurt product. Food Hydrocolloids. 2009;(2):490–6.

30.

Agostoni C, Turck D. Is cow’s milk harmful to a child’s health? Journal of Pediatric Gastroenterology and Nutrition. 2011;(6):594–600.

31.

Falony G, Vlachou A, Verbrugghe K, De Vuyst L. Cross-feeding between bifidobacterium longum bb536 and acetateconverting, butyrate-producing colon bacteria during growth on oligofructose. Applied and Environmental Microbiology. 2006;(12):7835–41.

32.

Garrido I, Monagas M, Gomez-Cordoves C, Bartolome B. Polyphenols and antioxidant properties of almond skins: influence of industrial processing. Journal of Food Science. 2008;(2):106-C115.

33.

Glahn R, Lee O, Yeung A, Goldman M, Miller D. Caco-2 cell ferritin formation predicts nonradiolabeled food iron availability in an in vitro digestion caco-2 cell culture model. Journal of Nutrition. 1998;(9):1555–61.

34.

Hoffman R. Intraepithelial lymphocytes coinduce nitric oxide synthase in in-testinal epithelial cells. American Journal of Physiology-gastrointestinal and Liver Physiology. 2000;(6):886-G894.

35.

Hu Z, Kobayashi K, Zenda N, Shimamura T. Tumor necrosis factoralpha-and interleukin-6-triggered mast cell development from mouse spleen cells. Blood. 1997;(2):526–33.

36.

Kabeerdoss J, Devi R, Mary R, Prabhavathi D, Vidya R, Mechenro J. Effect of yoghurt containing bifidobacterium lactis bb12 (r) on faecal excretion of secretory immunoglobulin a and human beta-defensin 2 in healthy adult volunteers. Nutrition Journal. 2011;10.

37.

Kalliomäki M. Probiotics, prebiotics synbiotics: a hope or hype in allergy? ical and Experimental Allergy. 2010;(5):694–6.

38.

Kalliomäki M, Antoine JM, Herz U, Rijkers G, Wells J, Mercenier A. 713S-721S. Workshop on Guidance for Assessing Probiotics Beneficial Effects -How to Fill the GAP, ILSI. Europe Assoc Int Dairy Federat. 2010;(3).

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