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Influence of bread crust-derived Maillard reaction products on phosphorus balance in rats

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Abstract

Background

Maillard reaction products (MRP) improve food palatability and are linked to some positive biological actions. However, diverse negative consequences, some related to protein damage and mineral availability, have been established.

Aim of study

We investigated the effects of MRP, from a bread crust diet, on phosphorus bioavailability and tissue distribution in rats to determine whether these effects are related to the molecular weight of browning products.

Methods

During a study period of 88 days, rats were fed either a control diet or one of the following: with bread crust as a source of MRP, or one with its soluble high molecular weight, soluble low molecular weight or insoluble fraction (bread crust, HMW, LMW and insoluble diets, respectively). In the final week, a phosphorus balance was performed, after which the animals were sacrificed and some organs removed to analyse phosphorus content. A second balance was carried out throughout the experimental period to calculate phosphorus retention.

Results

Phosphorus balance in the last week was unchanged. However, considering the whole experimental period, a trend towards improved bioavailability, significant in the HMW group, was observed. Higher phosphorus concentrations were measured in the small intestine and bone.

Conclusions

The consumption of MRP derived from bread did not alter phosphorus retention, due to increased bioavailability, especially concerning HMW compounds. The overall phosphorus body content remained unchanged and there were no changes in the bone, its principal metabolic destination. However, MRP consumption markedly raised phosphorus levels at the digestive level, especially when consumed as isolate fractions. The slower rate of stomach emptying is assumed to be related to this effect.

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References

  1. Ames JM (1998) Applications of the Maillard reaction in the food industry. Food Chem 62:431–439

    Article  CAS  Google Scholar 

  2. Jaeger H, Janositz A, Knorr D (2010) The Maillard reaction and its control during food processing. The potential of emerging technologies. Pathol Biol 58:207–213

    Article  CAS  Google Scholar 

  3. Prättälä RH, Helasoja V, Mykkänen H (2001) The consumption of rye bread and white bread as dimensions of health lifestyles in Finland. Public Health Nutr 4:7

    Article  Google Scholar 

  4. Siega-Riz AM, Poplin BM, Carson T (2000) Differences in food patterns at breakfast by sociodemographic characteristics among a nationally representative sample of adults in the United States. Prev Med 30:415–424

    Article  CAS  Google Scholar 

  5. Somoza V (2005) Five years of research on health risks and benefits of Maillard reaction products: an update. Mol Nutr Food Res 49:663–672

    Article  CAS  Google Scholar 

  6. Delgado-Andrade C, Morales FJ (2005) Unravelling the contribution of melanoidins to the antioxidant activity of coffee brews. J Agric Food Chem 53:1403–1407

    Article  CAS  Google Scholar 

  7. Marko D, Habermeyer M, Kemény M, Weyand U, Niederberger E, Frank O, Hofmann T (2003) Maillard reaction products modulating the growth of human tumor cells in vitro. Chem Res Toxicol 16:48–55

    Article  CAS  Google Scholar 

  8. Wagner KH, Reichhold S, Koschutnig K, Chériot S, Billaud C (2007) The potential antimutagenic and antioxidant effects of Maillard reaction products used as “natural antibrowning” agents. Mol Nutr Food Res 51:496–504

    Article  CAS  Google Scholar 

  9. Seiquer I, Díaz-Alguacil J, Delgado-Andrade C, López-Frías M, Muñoz Hoyos A, Galdó G, Navarro MP (2006) Diets rich in Maillard reaction products affect protein digestibility in adolescent males aged 11–14 y. Am J Clin Nutr 83:1082–1088

    CAS  Google Scholar 

  10. Navarro MP (2003) Impact of Maillard reaction products on mineral bioavailability. In: Vaquero MP, García-Arias T, Carbajal A, Sánchez-Múniz FJ (eds) Bioavailability of micronutrients and minor dietary compounds. Metabolic and technological aspects. Research Signpost, Kerala, pp 133–145

    Google Scholar 

  11. Rendleman JA (1987) Complexation of calcium by the melanoidin and its role in determining bioavailability. J Food Sci 52:1699–1705

    Article  CAS  Google Scholar 

  12. O’Brien J, Morrissey PA (1997) Metal ion complexation by products of the Maillard reaction. Food Chem 58:17–27

    Article  Google Scholar 

  13. Delgado-Andrade C, Seiquer I, Nieto R, Navarro MP (2004) Effects of heated glucose-lysine and glucose-methionine model systems on mineral solubility. Food Chem 87:329–337

    Article  CAS  Google Scholar 

  14. Morales FJ, Fernández-Fraguas C, Jiménez-Pérez S (2005) Iron-binding ability of melanoidins from food and model systems. Food Chem 90:821–827

    Article  CAS  Google Scholar 

  15. Andrieux C, Sacquet E (1984) Effects of Maillard’s reaction products on apparent mineral absorption in different parts of the digestive tract. The role of microflora. Reprod Nutr Develop 23:379–386

    Google Scholar 

  16. Knochel JP (1999) Phosphorus. In: Shils ME, Olson JA, Shike M, Catharine Ross A (eds) Modern nutrition in health and disease, 9th edn. Lippincott Williams & Wilkins, Pensylvania, pp 157–167

    Google Scholar 

  17. Drezner MK (2008) Phosphorus homeostasis and related disorders. In: Bilezikian JO, Raisz LG, Rodan RA (eds) Principles of bone biology, 3rd edn. Academic Press, San Diego, pp 465–486

  18. Delgado-Andrade C, Seiquer I, Mesías García M, Galdó G, Navarro MP (2011) Increased intake of Maillard reaction products reduces phosphorus digestibility in male adolescents. Nutrition 27:86–91

    Article  CAS  Google Scholar 

  19. Delgado-Andrade C, Rufián-Henares JA, Morales FJ (2008) Optimised procedure to analyse Maillard reaction-related fluorescence in cereal-based products. Czech J Food Sci 26:339–346

    CAS  Google Scholar 

  20. Reeves PG, Nielsen FH, Fahey GC (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951

    CAS  Google Scholar 

  21. AOAC (1980) In: Horwitz W (ed) Official methods of analysis, 13th edn. Association of Official Analytical Chemists, Washington, DC

  22. Delgado-Andrade C, Seiquer I, Haro A, Castellano R, Navarro MP (2010) Development of the Maillard reaction in foods cooked by different techniques. Intake of Maillard-derived compounds. Food Chem 122:145–153

    Article  CAS  Google Scholar 

  23. Seiquer I, Aspe T, Vaquero P, Navarro P (2001) Effects of heat treatment of casein in the presence of reducing sugars on calcium bioavailability: in vitro and in vivo assays. J Agric Food Chem 49:1049–1055

    Article  CAS  Google Scholar 

  24. Delgado-Andrade C, Seiquer I, Navarro MP (2002) Copper metabolism in rats fed diets containing Maillard reaction products. J Food Sci 67:855–860

    Article  CAS  Google Scholar 

  25. Mesías M, Seiquer I, Delgado-Andrade C, Galdó G, Navarro MP (2009) Intake of Maillard reaction products reduces iron bioavailability in male adolescents. Mol Nutr Food Res 53:1–10

    Google Scholar 

  26. Furniss DE, Vuichoud J, Finot PA, Hurrell RF (1989) The effect of Maillard reaction products on zinc metabolism in the rat. Br J Nutr 62:739–749

    Article  CAS  Google Scholar 

  27. Sarriá B, López-Fandino R, Vaquero MP (2001) Does processing of a powder or in-bottle-sterilized liquid infant formula affect calcium bioavailability? Nutrition 17:326–331

    Article  Google Scholar 

  28. Delgado-Andrade C (2002) Reacción de Maillard: Influencia sobre la biodisponibilidad mineral. Doctoral thesis, Granada, Spain

  29. Abu-Dweih BM, Tukan SK, Takruri HR (2000) The effect of browning intensity on the protein quality of qurshallah. Int J Food Sci Nutr 6:483–488

    Google Scholar 

  30. Andrieux E, Sacquet E, Guéguen L (1980) Interactions between Maillard reaction’s products, the microflora of the digestive tract and mineral metabolism. Reprod Nutr Develop 20(4):1061–1069

    Article  CAS  Google Scholar 

  31. Navarro P, Aspe T, Seiquer I (2002) Zinc transport in caco-2 cells and zinc balance in rats: influence of the heat treatment of a casein-glucose-fructose mixture. J Agric Food Chem 48:3589–3596

    Article  Google Scholar 

  32. Finot PA (2003) Toxicology of nonenzymatic browning. In: Caballero BC, Trugo LC, Finglas PM (eds) Encyclopedia of food sciences and nutrition, 2nd edn. Academic Press, London, pp 673–678

  33. Friedman M (1996) Food browning and its prevention: an overview. J Agric Food Chem 44:631–653

    Article  CAS  Google Scholar 

  34. Somoza V, Lindenmeier M, Hofmann T, Frank O, Erbersdobler HF, Baynes JW et al (2005) Dietary bread crust advanced glycation end products bind to the receptor for AGEs in HEK-293 kidney cells but are rapidly excreted after oral administration to healthy and subtotally nephrectomized rats. Ann NY Acad Sci 1043:492–500

    Article  CAS  Google Scholar 

  35. Kutchai HC (1998) Gastrointestinal secretion. In: Berne RM, Levy MN, Koeppen BM, Stanton BA (eds) Physiology, 4th edn. Mosby Inc., St. Louis, pp 617–646

    Google Scholar 

  36. Rèrat A, Calmes R, Vaissade P, Finot PA (2002) Nutritional and metabolic consequences of the early Maillard reaction of heat treated milk in the pig, significance for man. Eur J Nutr 41:1–11

    Google Scholar 

  37. Kimiagar M, Lee TC, Chichester CO (1980) Long-term feeding effects of browned egg albumin to rats. J Agric Food Chem 28:150–155

    Article  CAS  Google Scholar 

  38. Somoza V, Wenzel E, Lindenmeier M, Grothe D, Erbersdobler HF, Hofman T (2005) Influence of feeding malt, bread crust, and a pronylated protein on the activity of chemopreventive enzymes and antioxidative defense parameters in vivo. J Agric Food Chem 53:8176–8182

    Article  CAS  Google Scholar 

  39. Bovee-Oudehoven IM, Wissink ML, Wouters JT, Van der Meer R (1999) Dietary calcium phosphate stimulates intestinal Lactobacilli and decreases the severity of a Salmonella infection in rats. J Nutr 129:607–612

    Google Scholar 

  40. Hein GE (2006) Glycation endproducts in osteoporosis—is there a pathophysiologic importance? Clin Chim Acta 371:32–36

    Article  CAS  Google Scholar 

  41. Alikhani M, Alikhani Z, Boyd C, MacLellan CM, Raptis M, Liu R, Pischon N, Trackman PC, Gerstenfeld L, Graves DT (2007) Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone 40:345–353

    Article  CAS  Google Scholar 

  42. Kawashima Y, Fritton JC, Yakar S, Epstein S, Schaffler MB, Jepsen KJ, LeRoith D (2009) Type 2 diabetic mice demonstrate slender long bones with increased fragility secondary to increased osteoclastogenesis. Bone 44:648–665

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by a project of the Spanish Ministry of Science and Innovation. The authors thank Grupo Siro, a Spanish manufacturer of cereal-derived food products, for supplying the bread crust samples.

Conflict of interest

The authors declare there is no conflict of interest.

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Authors and Affiliations

  1. Instituto en Formación de Nutrición Animal, Estación Experimental del Zaidín, CSIC, Camino del Jueves s/n, 18100, Armilla, Granada, Spain

    Irene Roncero-Ramos, Cristina Delgado-Andrade, Rebeca Alonso-Olalla & María Pilar Navarro

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  1. Irene Roncero-Ramos
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  2. Cristina Delgado-Andrade
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  3. Rebeca Alonso-Olalla
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  4. María Pilar Navarro
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Correspondence to Cristina Delgado-Andrade.

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Roncero-Ramos, I., Delgado-Andrade, C., Alonso-Olalla, R. et al. Influence of bread crust-derived Maillard reaction products on phosphorus balance in rats. Eur J Nutr 51, 871–879 (2012). https://doi.org/10.1007/s00394-011-0267-3

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  • DOI: https://doi.org/10.1007/s00394-011-0267-3

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