Advertisement

Modification of Milk Fat Globules During Processing and Gastrointestinal Digestion

  • Sophie Gallier
  • Harjinder SinghEmail author
Chapter
  • 133 Downloads

Abstract

Milk is an important source of nutrition in the diet of children and adults. Our understanding of the structure of the milk fat globules and the effect of dairy processing on the digestion of lipids has increased over the last decades. The role of the milk fat globule membrane (MFGM) has moved beyond being simply a triglyceride-stabilizing membrane and is recognized for providing efficient digestion, gut maturation and protection and brain development. This chapter reviews the structure of the MFGM, the effect of processing on the structure of the fat globules and impact on their digestion under adult and infant conditions, and the development of emulsions mimicking the structure of milk fat globules.

References

  1. Armand, M., Hamosh, M., Mehta, N. R., Angelus, P. A., Philpott, J. R., Henderson, T. R., et al. (1996). Effect of human milk or formula on gastric function and fat digestion in the premature infant. Pediatric Research, 40, 429–437.PubMedCrossRefGoogle Scholar
  2. Baars, A., Oosting, A., Engels, E., Kegler, D., Kodde, A., Schipper, L., et al. (2016). Milk fat globule membrane coating of large lipid droplets in the diet of young mice prevents body fat accumulation in adulthood. British Journal of Nutrition, 115, 1930–1937.PubMedCrossRefGoogle Scholar
  3. Baumgartner, S., van de Heijning, B. J. M., Acton, D., & Mensink, R. P. (2017). Infant milk fat droplet size and coating affect postprandial responses in healthy adult men: A proof-of-concept study. European Journal of Clinical Nutrition, 71, 1108–1113.PubMedCrossRefGoogle Scholar
  4. Berton, A., Sebban-Kreuzer, C., Rouvellac, S., Lopez, C., & Crenon, I. (2009). Individual and combined action of pancreatic lipase and pancreatic lipase-related proteins 1 and 2 on native versus homogenized milk fat globules. Molecular Nutrition & Food Research, 53, 1592–1602.CrossRefGoogle Scholar
  5. Billeaud, C., Guillet, J., & Sandler, B. (1990). Gastric emptying in infants with or without gastro-oesophageal reflux according to the type of milk. European Journal of Clinical Nutrition, 44, 577–583.PubMedGoogle Scholar
  6. Borgstrom, B., & Erlanson-Albertsson, C. (1982). Hydrolysis of milk fat globules by pancreatic lipase – Role of colipase, phospholipase A2, and bile salts. Journal of Clinical Investigation, 70, 30–32.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bourlieu, C., & Michalski, M.-C. (2015). Structure–function relationship of the milk fat globule. Current Opinion in Clinical Nutrition & Metabolic Care, 18, 118–127.CrossRefGoogle Scholar
  8. Bourlieu, C., Menard, O., De La Chevasnerie, A., Sams, L., Rousseau, F., Madec, M. N., et al. (2015). The structure of infant formulas impacts their lipolysis, proteolysis and disintegration during in vitro gastric digestion. Food Chemistry, 182, 224–235.PubMedCrossRefGoogle Scholar
  9. Bourlieu, C., Paboeuf, G., Chever, S., Pezennec, S., Cavalier, J. F., Guyomarc’h, F., et al. (2016). Adsorption of gastric lipase onto multicomponent model lipid monolayers with phase separation. Colloids and Surfaces B: Biointerfaces, 143, 97–106.PubMedCrossRefGoogle Scholar
  10. Buchheim, W., Welsch, U., Huston, G. E., & Patton, S. (1988). Glycoprotein filament removal from human milk fat globules by heat treatment. Pediatrics, 81, 141–146.PubMedGoogle Scholar
  11. Carnielli, V. P., Luijendijk, I. H., Van Goudoever, J. B., Sulkers, E. J., Boerlage, A. A., Degenhart, H. J., et al. (1996). Structural position and amount of palmitic acid in infant formulas: Effects on fat, fatty acid, and mineral balance. Journal of Pediatric Gastroenterology and Nutrition, 23, 553–560.PubMedCrossRefGoogle Scholar
  12. Cavell, B. (1981). Gastric emptying in infants fed human milk or infant formula. Acta Paediatrica Scandinavica, 70, 639–641.PubMedCrossRefGoogle Scholar
  13. Chu, B. S., Gunning, A. P., Rich, G. T., Ridout, M. J., Faulks, R. M., Wickham, M. S. J., et al. (2010). Adsorption of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol and dipalmitoylphosphatidylcholine monolayers. Langmuir, 26, 9782–9793.PubMedCrossRefGoogle Scholar
  14. Cilla, A., Quintaes, K. D., Barberá, R., & Alegría, A. (2016). Phospholipids in human milk and infant formulas: Benefits and needs for correct infant nutrition. Critical Reviews in Food Science and Nutrition, 56, 1880–1892.PubMedCrossRefGoogle Scholar
  15. Claumarchirant, L., Matencio, E., Sanchez-Siles, L. M., Alegría, A., & Lagarda, M. J. (2015). Sterol composition in infant formulas and estimated intake. Journal of Agricultural and Food Chemistry, 63, 7245–7251.PubMedCrossRefGoogle Scholar
  16. Claumarchirant, L., Cilla, A., Matencio, E., Sanchez-Siles, L. M., Castro-Gomez, P., Fontecha, J., et al. (2016). Addition of milk fat globule membrane as an ingredient of infant formulas for resembling the polar lipids of human milk. International Dairy Journal, 61, 228–238.CrossRefGoogle Scholar
  17. Contarini, G., & Povolo, M. (2013). Phospholipids in milk fat: Composition, biological and technological significance, and analytical strategies. International Journal of Molecular Science, 14, 2808–2831.CrossRefGoogle Scholar
  18. Corredig, M., & Dalgleish, D. G. (1997). Isolates from industrial buttermilk: Emulsifying properties of materials derived from the milk fat globule membrane. Journal of Agricultural and Food Chemistry, 45, 4595–4600.CrossRefGoogle Scholar
  19. Corredig, M., & Dalgleish, D. G. (1998). Effect of heating of cream on the properties of milk fat globule membrane isolates. Journal of Agricultural and Food Chemistry, 46, 2533–2540.CrossRefGoogle Scholar
  20. Couvreur, S., Hurtaud, C., Lopez, C., Delaby, L., & Peyraud, J. L. (2006). The linear relationship between the proportion of fresh grass in the cow diet, milk fatty acid composition, and butter properties. Journal of Dairy Science, 89, 1956–1969.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Cruz, M. L., Wong, W. W., Mimouni, F., Hachey, D. L., Setchell, K. D., Klein, P. D., et al. (1994). Effects of infant nutrition on cholesterol synthesis rates. Pediatric Research, 35, 135–140.PubMedCrossRefGoogle Scholar
  22. de Oliveira, S. C., Deglaire, A., Menard, O., Bellanger, A., Rousseau, F., Henry, G., et al. (2015). Holder pasteurization impacts the proteolysis, lipolysis and disintegration of human milk under in vitro dynamic term newborn digestion. Food Research International, 88(Part B), 263–275.Google Scholar
  23. de Oliveira, S. C., Menard, O., Bellanger, A., Henry, G., Rousseau, F., Dirson, E., et al. (2016). Impact of pasteurization of human milk on preterm newborn in vitro digestion: Gastrointestinal disintegration, lipolysis and proteolysis. Food Chemistry, 211, 171–179.PubMedCrossRefGoogle Scholar
  24. de Oliveira, S. C., Bellanger, A., Menard, O., Pladys, P., Le Gouar, Y., Dirson, E., et al. (2017). Impact of human milk pasteurization on gastric digestion in preterm infants: A randomized controlled trial. American Journal of Clinical Nutrition, 105, 379–390.PubMedCrossRefGoogle Scholar
  25. Demmer, E., Van Loan, M. D., Rivera, N., Rogers, T. A., Gertz, E. R., German, B., et al. (2016). Addition of a dairy fraction rich in milk fat globule membrane to a high-saturated fat meal reduces the postprandial insulinaemic and inflammatory response in overweight and obese adults. Journal of Nutritional Science, 5.  https://doi.org/10.1017/jns.2015.42
  26. Fong, B. Y., & Norris, C. S. (2009). Quantification of milk fat globule membrane proteins using selected reaction monitoring mass spectrometry. Journal of Agricultural and Food Chemistry, 57, 6021–6028.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Fong, B., Ma, L., & Norris, C. (2013). Analysis of phospholipids in infant formulas using high performance liquid chromatography–tandem mass spectrometry. Journal of Agricultural and Food Chemistry, 61, 858–865.PubMedCrossRefGoogle Scholar
  28. Gallier, S., Gragson, D., Jimenez-Flores, R., & Everett, D. W. (2010a). Using confocal laser scanning microscopy to probe the milk fat globule membrane and associated proteins. Journal of Agricultural and Food Chemistry, 58, 4250–4257.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Gallier, S., Gragson, D., Jimenez-Flores, R., & Everett, D. W. (2010b). Surface characterization of bovine milk phospholipid mono layers by Langmuir isotherms and microscopic techniques. Journal of Agricultural and Food Chemistry, 58, 12275–12285.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Gallier, S., Gragson, D., Jimenez-Flores, R., & Everett, D. W. (2012). β-Casein–phospholipid monolayers as model systems to understand lipid–protein interactions in the milk fat globule membrane. International Dairy Journal, 22, 58–65.Google Scholar
  31. Gallier, S., Cui, J., Olson, T. D., Rutherfurd, S. M., Ye, A., Moughan, P. J., et al. (2013a). In vivo digestion of bovine milk fat globules: Effect of processing and interfacial structural changes. I. Gastric digestion. Food Chemistry, 141, 3273–3281.PubMedCrossRefGoogle Scholar
  32. Gallier, S., Zhu, X. Q., Rutherfurd, S. M., Ye, A., Moughan, P. J., & Singh, H. (2013b). In vivo digestion of bovine milk fat globules: Effect of processing and interfacial structural changes. II. Upper digestive tract digestion. Food Chemistry, 141, 3215–3223.PubMedCrossRefGoogle Scholar
  33. Gallier, S., Rutherfurd, S. M., Moughan, P. J., & Singh, H. (2014a). Effect of food matrix microstructure on stomach emptying rate and apparent ileal fatty acid digestibility of almond lipids. Food and Function, 5, 2410–2419.PubMedCrossRefGoogle Scholar
  34. Gallier, S., Shaw, E., Laubscher, A., Gragson, D., Singh, H., & Jimenez-Flores, J. (2014b). Adsorption of bile salts to milk phospholipid and phospholipid-protein monolayers. Journal of Agricultural and Food Chemistry, 62, 1363–1372.PubMedCrossRefGoogle Scholar
  35. Gallier, S., Vocking, K., Post, J. A., Acton, D., Van Der Beek, E. M., & Van Baalen, T. (2015). A novel infant milk formula concept: Mimicking the human milk fat globule structure. Colloids and Surfaces B: Biointerfaces, 136, 329–339.PubMedCrossRefGoogle Scholar
  36. Gallier, S., Acton, D., Manohar, G., & Singh, H. (2017). Natural and processed milk and oil body emulsions: Bioavailability, bioaccessibility and functionality. Food Structure, 13, 13–23.CrossRefGoogle Scholar
  37. Gurnida, D. A., Rowan, A. M., Idjradinata, P., Muchtadi, D., & Sekarwana, N. (2012). Association of complex lipids containing gangliosides with cognitive development of 6-month-old infants. Early Human Development, 88, 595–601.PubMedCrossRefGoogle Scholar
  38. Hernell, O., Timby, N., Domellof, M., & Lonnerdal, B. (2016). Clinical benefits of milk fat globule membranes for infants and children. Journal of Pediatrics, 173, S60–S65.PubMedCrossRefGoogle Scholar
  39. Houlihan, A. V., Goddard, P. A., Kitchen, B. J., & Masters, C. J. (1992). Changes in structure of the bovine milk fat globule membrane on heating whole milk. Journal of Dairy Research, 59, 321–329.PubMedCrossRefGoogle Scholar
  40. Huang, S., Mo, T. T., Norris, T., Sun, S., Zhang, T., Han, T. L., et al. (2017). The CLIMB (Complex Lipids In Mothers and Babies) study: Protocol for a multicentre, three-group, parallel randomised controlled trial to investigate the effect of supplementation of complex lipids in pregnancy, on maternal ganglioside status and subsequent cognitive outcomes in the offspring. BMJ Open, 7, e016637.PubMedPubMedCentralGoogle Scholar
  41. Huston, G. E., & Patton, S. (1990). Factors related to the formation of cytoplasmic crescents on milk fat globules. Journal of Dairy Science, 73, 2061–2066.PubMedCrossRefGoogle Scholar
  42. Innis, S. M. (2011). Dietary triacylglycerol structure and its role in infant nutrition. Advances in Nutrition, 2, 275–283.PubMedPubMedCentralCrossRefGoogle Scholar
  43. Islam, M. A., Devle, H., Comi, I., Ulleberg, E. K., Rukke, E.-O., Vegarud, G. E., et al. (2017). Ex vivo digestion of raw, pasteurised and homogenised milk – effects on lipolysis and proteolysis. International Dairy Journal, 65, 14–19.CrossRefGoogle Scholar
  44. Jensen, R. J., & Newsburg, D. S. (1995). Bovine milk lipids. In G. J. Robert (Ed.), Handbook of milk composition (pp. 543–575). San Diego, CA: Academic.CrossRefGoogle Scholar
  45. Keenan, T. W., & Dylewski, D. P. (1995). Intracellular origin of milk lipid globules and the nature and structure of the milk lipid globule membrane. In P. F. Fox (Ed.), Advanced dairy chemistry. Lipids (Vol. 2, pp. 137–171). London: Chapman & Hall.Google Scholar
  46. Kim, H. H. Y., & Jimenez-Flores, R. (1995). Heat-induced interactions between the proteins of milk fat globule membrane and skim milk. Journal of Dairy Science, 78, 24–35.PubMedCrossRefGoogle Scholar
  47. Koletzko, B. (2016). Human milk lipids. Annals of Nutrition and Metabolism, 69(Suppl 2), 28–40.PubMedCrossRefGoogle Scholar
  48. Kuchta, A. M., Kelly, P. M., Stanton, C., & Devery, R. A. (2012). Milk fat globule membrane – A source of polar lipids for colon health? A review. International Journal of Dairy Technology, 65, 315–333.CrossRefGoogle Scholar
  49. Le, T. T., Van de Wiele, T., Do, T. N. H., Debyser, G., Struijs, K., Devreese, B., et al. (2012). Stability of milk fat globule membrane proteins toward human enzymatic gastrointestinal digestion. Journal of Dairy Science, 95, 2307–2318.PubMedCrossRefGoogle Scholar
  50. Le Huërou-Luron, I., Bouzerzour, K., Ferret-Bernard, S., Menard, O., Le Normand, L., Perrier, C., et al. (2018). A mixture of milk and vegetable lipids in infant formula changes gut digestion, mucosal immunity and microbiota composition in neonatal piglets. European Journal of Nutrition, 57, 463–476.PubMedCrossRefGoogle Scholar
  51. Lecomte, M., Bourlieu, C., Meugnier, E., Penhoat, A., Cheillan, D., Pineau, G., et al. (2015). Milk polar lipids affect in vitro digestive lipolysis and postprandial lipid metabolism in mice. Journal of Nutrition, 145, 1770–1777.PubMedCrossRefGoogle Scholar
  52. Lepri, L., Del Bubba, M., Maggini, R., Donzelli, G. P., & Galvan, P. (1997). Effect of pasteurization and storage on some components of pooled human milk. Journal of Chromatography B Biomedical Sciences and Application, 704, 1–10.CrossRefGoogle Scholar
  53. Lindquist, S., & Hernell, O. (2010). Lipid digestion and absorption in early life: An update. Current Opinion in Clinical Nutrition & Metabolic Care, 13, 314–320.CrossRefGoogle Scholar
  54. Lopez, C., Madec, M. N., & Jimenez-Flores, R. (2010). Lipid rafts in the bovine milk fat globule membrane revealed by the lateral segregation of phospholipids and heterogeneous distribution of glycoproteins. Food Chemistry, 120, 22–33.CrossRefGoogle Scholar
  55. Lopez, C., Cauty, C., & Guyomarc’h, F. (2015). Organization of lipids in milks, infant milk formulas and various dairy products: Role of technological processes and potential impacts. Dairy Science & Technology, 95, 863–893.CrossRefGoogle Scholar
  56. Lopez, C., Cauty, C., Rousseau, F., Blot, M., Margolis, A., & Famelart, M.-H. (2017). Lipid droplets coated with milk fat globule membrane fragments: Microstructure and functional properties as a function of pH. Food Research International, 91, 26–37.CrossRefPubMedGoogle Scholar
  57. Maldonado-Valderrama, J., Wilde, P., Macierzanka, A., & Mackie, A. (2011). The role of bile salts in digestion. Advances in Colloid and Interface Science, 165, 36–46.PubMedCrossRefGoogle Scholar
  58. Marciani, L., Wickham, M., Sing, G., Bush, D., Pick, B., Cox, E., et al. (2007). Enhancement of intragastric acid stability of a fat emulsion meal delays gastric emptying and increases cholecystokinin release and gallbladder contraction. American Journal of Physiology – Gastrointestinal and Liver Physiology, 292, G1607–G1613.PubMedCrossRefGoogle Scholar
  59. Martini, M., Salari, F., & Altomonte, I. (2016). The macrostructure of milk lipids: The fat globules. Critical Review in Food Science and Nutrition, 56, 209–221.CrossRefGoogle Scholar
  60. Masedunskas, A., Weigert, R., & Mather, I. H. (2014). Chapter 9 – Intravital imaging of the lactating mammary gland in transgenic mice expressing fluorescent proteins. In R. Weigert (Ed.), Advances in intravital microscopy: From basic to clinical research (pp. 187–204). Dordrecht: Springer Science+Business Media.Google Scholar
  61. Masedunskas, A., Chen, Y., Stussman, R., Weigert, R., & Mather, I. H. (2017). Kinetics of milk lipid droplet transport, growth, and secretion revealed by intravital imaging: Lipid droplet release is intermittently stimulated by oxytocin. Molecular Biology of the Cell, 28, 935–947.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Mathiassen, J. H., Nejrup, R. G., Frøkiær, H., Nilsson, Å., Ohlsson, L., & Hellgren, L. I. (2015). Emulsifying triglycerides with dairy phospholipids instead of soy lecithin modulates gut lipase activity. European Journal of Lipid Science & Technology, 117, 1522–1539.CrossRefGoogle Scholar
  63. Ménard, O., Bourlieu, C., De Oliveira, S. C., Dellarosa, N., Laghi, L., Carrière, F., et al. (2018). A first step towards a consensus static in vitro model for simulating full-term infant digestion. Food Chemistry, 240, 338–345.PubMedCrossRefGoogle Scholar
  64. Mendez-Otero, R., Pimentel-Coelho, P. M., Ukraintsev, S., & McJarrow, P. (2013). Chapter 9 – Role of gangliosides in neurological development and the influence of dietary sources. In R. R. Watson et al. (Eds.), Nutrition in infancy (Vol. 2, pp. 105–118). New York, NY: Nutrition and Health, Springer Science+Business Media.CrossRefGoogle Scholar
  65. Michalski, M.-C., Briard, V., Desage, M., & Geloen, A. (2005). The dispersion state of milk fat influences triglyceride metabolism in the rat – A (CO2)-C13 breath test study. European Journal of Nutrition, 44, 436–444.PubMedCrossRefGoogle Scholar
  66. Michalski, M.-C., Soares, A. F., Lopez, C., Leconte, N., Briard, V., & Geloen, A. (2006). The supramolecular structure of milk fat influences plasma triacylglycerols and fatty acid profile in the rat. European Journal of Nutrition, 45, 215–224.PubMedCrossRefGoogle Scholar
  67. Miklavcic, J. J., Schnabl, K. L., Mazurak, V. C., Thomson, A. B. R., & Clandinin, M. T. (2012). Dietary ganglioside reduces proinflammatory signaling in the intestine. Journal of Nutrition and Metabolism, 2012, 280–286.CrossRefGoogle Scholar
  68. Murthy, A. V. R., Guyomarc’h, F., Paboeuf, G., Vié, V., & Lopez, C. (2015). Cholesterol strongly affects the organization of lipid monolayers studied as models of the milk fat globule membrane: Condensing effect and change in the lipid domain morphology. Biochimica et Biophysica Acta, 1848, 2308–2316.Google Scholar
  69. N’Goma, J.-C. B., Amara, S., Dridi, K., Jannin, V., & Carrière, F. (2012). Understanding the lipid-digestion processes in the GI tract before designing lipid-based drug-delivery systems. Therapeutic Delivery, 3, 105–124.CrossRefGoogle Scholar
  70. Oftedal, O. T. (2012). The evolution of milk secretion and its ancient origins. Animal, 6, 355–368.PubMedCrossRefGoogle Scholar
  71. Oosting, A., Kegler, D., Woopereis, H. J., Teller, I. C., Van De Heijning, B. J. M., Verkade, H. J., et al. (2012). Size and phospholipid coating of lipid droplets in the diet of young mice modify body fat accumulation in adulthood. Pediatric Research, 72, 362–369.PubMedCrossRefGoogle Scholar
  72. Oosting, A., Van Vlies, N., Kegler, D., Schipper, L., Abrahamse-Berkeveld, M., Ringler, S., et al. (2014). Effect of dietary lipid structure in early postnatal life on mouse adipose tissue development and function in adulthood. British Journal of Nutrition, 111, 215–226.PubMedCrossRefGoogle Scholar
  73. Patton, S., Borgstrom, B., Stemberger, B. H., & Welsch, U. (1986). Release of membrane from milk-fat globules by conjugated bile-salts. Journal of Pediatric Gastroenterology and Nutrition, 5, 262–267.PubMedCrossRefGoogle Scholar
  74. Patton, S., & Huston, G. E. (1988). Incidence and characteristics of cell pieces on human milk fat globules. Biochimica et Biophysica Acta – General Subjects, 965, 146–153.CrossRefGoogle Scholar
  75. Rosqvist, F., Smedman, A., Lindmark-Mansson, H., Paulsson, M., Petrus, P., Straniero, S., et al. (2015). Potential role of milk fat globule membrane in modulating plasma lipoproteins, gene expression, and cholesterol metabolism in humans: A randomized study. American Journal of Clinical Nutrition, 102, 20–30.PubMedCrossRefGoogle Scholar
  76. Sams, L., Paume, J., Giallo, J., & Carriere, F. (2016). Relevant pH and lipase for in vitro models of gastric digestion. Food & Function, 7, 30–45.CrossRefGoogle Scholar
  77. Sarkar, A., Goh, K. K. T., & Singh, H. (2009). Colloidal stability and interactions of milk-protein-stabilized emulsions in an artificial saliva. Food Hydrocolloids, 23, 1270–1278.CrossRefGoogle Scholar
  78. Shani-Levi, C., Alvito, P., Andres, A., Assuncao, R., Barbera, R., Blanquet-Diot, S., et al. (2017). Extending in vitro digestion models to specific human populations: Perspectives, practical tools and bio-relevant information. Trends in Food Science & Technology, 60, 52–63.CrossRefGoogle Scholar
  79. Singh, H. (2006). The milk fat globule membrane – A biophysical system for food applications. Current Opinion in Colloid & Interface Science, 11, 154–163.CrossRefGoogle Scholar
  80. Singh, H., & Gallier, S. (2014). Chapter 2 – Processing of food structures in the gastrointestinal tract and physiological responses. In Food structures, digestion and health (pp. 51–81). San Diego, CA: Academic.CrossRefGoogle Scholar
  81. Singh, H., & Gallier, S. (2016). Nature’s complex emulsion: The fat globules of milk. Food Hydrocolloids, 68, 81–89.Google Scholar
  82. Sousa, S. G., Delgadillo, I., & Saraiva, J. A. (2016). Human milk composition and preservation: Evaluation of high-pressure processing as a nonthermal pasteurization technology. Critical Reviews in Food Science and Nutrition, 56, 1043–1060.PubMedCrossRefGoogle Scholar
  83. Tanaka, K., Hosozawa, M., Kudo, N., Yoshikawa, N., Hisata, K., Shoji, H., et al. (2013). The pilot study: Sphingomyelin-fortified milk has a positive association with the neurobehavioural development of very low birth weight infants during infancy, randomized control trial. Brain & Development, 35, 45–52.CrossRefGoogle Scholar
  84. Timby, N., Domellof, E., Hernell, O., Lonnerdal, B., & Domellof, M. (2014). Neurodevelopment, nutrition, and growth until 12 mo of age in infants fed a low-energy, low-protein formula supplemented with bovine milk fat globule membranes: A randomized controlled trial. American Journal of Clinical Nutrition, 99, 860–868.PubMedCrossRefGoogle Scholar
  85. Timby, N., Hernell, O., Vaarala, O., Melin, M., Lonnerdal, B., & Domellof, M. (2015). Infections in infants fed formula supplemented with bovine milk fat globule membranes. Journal of Pediatric Gastroenterology and Nutrition, 60, 384–389.PubMedCrossRefGoogle Scholar
  86. Timby, N., Domellof, M., Lonnerdal, B., & Hernell, O. (2017). Supplementation of infant formula with bovine milk fat globule membranes. Advances in Nutrition, 8, 351–355.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Tunick, M. H., Ren, D. X., Van Hekken, D. L., Bonnaillie, L., Paul, M., Kwoczak, R., et al. (2016). Effect of heat and homogenization on in vitro digestion of milk. Journal of Dairy Science, 99, 4124–4139.PubMedCrossRefGoogle Scholar
  88. van de Heijning, B. J. M., Berton, A., Bouritius, H., & Goulet, O. (2014). GI symptoms in infants are a potential target for fermented infant milk formulae: A review. Nutrients, 6, 3942–3967.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Veereman-Wauters, G., Staelens, S., Rombaut, R., Dewettinck, K., Deboutte, D., Brummer, R. J., et al. (2012). Milk fat globule membrane (INPULSE) enriched formula milk decreases febrile episodes and may improve behavioral regulation in young children. Nutrition, 28, 749–752.PubMedCrossRefGoogle Scholar
  90. Vieira, A. A., Mendes Soares, F. V., Porto Pimenta, H., Abranches, A. D., & Lopes Moreira, M. E. (2011). Analysis of the influence of pasteurization, freezing/thawing, and offer processes on human milk’s macronutrient concentrations. Early Human Development, 87, 577–580.PubMedCrossRefGoogle Scholar
  91. Vors, C., Pineau, G., Gabert, L., Drai, J., Louche-Pelissier, C., Defoort, C., et al. (2013). Modulating absorption and postprandial handling of dietary fatty acids by structuring fat in the meal: A randomized crossover clinical trial. American Journal of Clinical Nutrition, 97, 23–36.PubMedCrossRefGoogle Scholar
  92. Walstra, P. (1995). Chapter 4 – Physical chemistry of milk fat globules. In P. F. Fox (Ed.), Advanced dairy chemistry. Lipids (Vol. 2, pp. 131–178). London: Chapman & Hall.Google Scholar
  93. Walstra, P., Wouters, J. T. M., & Geurts, T. J. (2006). Dairy science and technology (p. 756). Boca Raton, FL: Taylor & Francis Group.Google Scholar
  94. Wang, M., & Donovan, S. M. (2015). Human microbiota-associated swine: Current progress and future opportunities. ILAR Journal, 56, 63–73.PubMedPubMedCentralCrossRefGoogle Scholar
  95. Ye, A., Singh, H., Taylor, M. W., & Anema, S. (2002). Characterization of protein components of natural and heat-treated milk fat globule membranes. International Dairy Journal, 12, 393–402.CrossRefGoogle Scholar
  96. Ye, A. Q., Singh, H., Taylor, M. W., & Anema, S. (2004). Interactions of whey proteins with milk fat globule membrane proteins during heat treatment of whole milk. Le Lait, 84, 269–283.CrossRefGoogle Scholar
  97. Ye, A., Cui, J., & Singh, H. (2010). Effect of the fat globule membrane on in vitro digestion of milk fat globules with pancreatic lipase. International Dairy Journal, 20, 822–829.CrossRefGoogle Scholar
  98. Ye, A., Cui, J., & Singh, H. (2011). Proteolysis of milk fat globule membrane proteins during in vitro gastric digestion of milk. Journal of Dairy Science, 94, 2762–2770.PubMedCrossRefGoogle Scholar
  99. Ye, A., Cui, J., Dalgleish, D., & Singh, H. (2016). Formation of a structured clot during the gastric digestion of milk: Impact on the rate of protein hydrolysis. Food Hydrocolloids, 52, 478–486.CrossRefGoogle Scholar
  100. Ye, A., Cui, J., Dalgleish, D., & Singh, H. (2017). Effect of homogenization and heat treatment on the behaviour of protein and fat globules during gastric digestion of milk. Journal of Dairy Science, 100, 36–47.PubMedCrossRefGoogle Scholar
  101. Zavaleta, N., Kvistgaard, A. S., Graverholt, G., Respicio, G., Guija, H., Valencia, N., et al. (2011). Efficacy of an MFGM-enriched complementary food in diarrhea, anemia, and micronutrient status in infants. Journal of Pediatric Gastroenterology and Nutrition, 53, 561–568.PubMedGoogle Scholar
  102. Zheng, H., Jiménez-Flores, R., Gragson, D., & Everett, D. W. (2014). Phospholipid architecture of the bovine milk fat globule membrane using giant unilamellar vesicles as a model. Journal of Agricultural and Food Chemistry, 62, 3236–3243.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Fonterra Research and Development CentreFonterra Co-operative Group LtdPalmerston NorthNew Zealand
  2. 2.Riddet Institute and Massey Institute of Food Science and Technology, Massey UniversityPalmerston NorthNew Zealand

Personalised recommendations