Bovine colostrum is superior to enriched formulas in stimulating intestinal function and necrotising enterocolitis resistance in preterm pigs

British Journal of Nutrition

Volumn 105, Issue 1, 2011, Pages 44-53

  Moøller, Hanne K ^a,b   Thymann, Thomas ^b   Fink, Lisbeth N ^a   Frokiaer, Hanne ^b   Kvistgaard, Anne S ^c   Sangild, Per T ^b  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c Arla Foods   (Denmark)

Author keywords

Colostrum; Immunomodulation; Milk bioactives; Necrotising enterocolitis

Indexed keywords

ALPHA GLUCOSIDASE; AMINOPEPTIDASE; DIPEPTIDYL PEPTIDASE IV; GANGLIOSIDE; HEXOSE; LACTASE; MONOUNSATURATED FATTY ACID; OSTEOPONTIN; POLYUNSATURATED FATTY ACID; SATURATED FATTY ACID; SIALIC ACID; SUCRASE;

ANIMAL EXPERIMENT; ARTICLE; ARTIFICIAL MILK; CARBOHYDRATE ABSORPTION; CESAREAN SECTION; COLOSTRUM; CONTROLLED STUDY; CYTOKINE RESPONSE; DENDRITIC CELL; DOSE RESPONSE; ENTERIC FEEDING; ENZYME ACTIVITY; FOOD COMPOSITION; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; INTESTINE FUNCTION; INTESTINE MUCOSA; NECROTIZING ENTEROCOLITIS; NONHUMAN; PREMATURITY; SWINE; TOTAL PARENTERAL NUTRITION; WHEY;

ANIMALS; ANIMALS, NEWBORN; BACTERIA; BONE MARROW; CATTLE; CELL LINE; COLOSTRUM; CYTOKINES; DENDRITIC CELLS; DIGESTION; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENTEROCOLITIS, NECROTIZING; FEMALE; FOOD, FORMULATED; FOOD, FORTIFIED; GANGLIOSIDES; INTESTINE, SMALL; MILK; MILK PROTEINS; NUTRITIONAL SUPPORT; OSTEOPONTIN; PREGNANCY; PREMATURE BIRTH; SIALIC ACIDS; SWINE;

BOVINAE; MURINAE; SUIDAE;

EID: 79951676297     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114510003168     Document Type: Article

References (52)

1. Kelleher SL & Lönnerdal B (2001) Immunological activities associated with milk. Adv Nutr Res 10, 39-65.
2. Field CJ (2005) The immunological components of human milk and their effect on immune development in infants. J Nutr 135, 1-4. (Pubitemid 40094311)
3. Edwards CA & Parrett AM (2002) Intestinal flora during the first months of life: new perspectives. Br J Nutr 88, S11-S18. (Pubitemid 35251939)
4. Ashkar S, Weber GF, Panoutsakopoulou V, et al. (2000) Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science 287, 860-864. (Pubitemid 30084330)
5. Begum MD, Umemura M, Kon S, et al. (2007) Suppression of the bacterial antigen-specific T cell response and the dendritic cell migration to the lymph nodes by osteopontin. Microbiol Immunol 51, 135-147. (Pubitemid 46155196)
6. Boehm G, Lidestri M, Casetta P, et al. (2002) Supplementation of a bovine milk formula with an oligosaccharide mixture increases counts of faecal bifidobacteria in preterm infants. Arch Dis Child 86, 178-181.
7. Martin MJ, Martin-Sosa S, Alonso JM, et al. (2003) Enterotoxigenic Escherichia coli strains bind bovine milk gangliosides in a ceramide-dependent process. Lipids 38, 761-768. (Pubitemid 37362268)
8. Renkl AC, Wussler J, Ahrens T, et al. (2005) Osteopontin functionally activates dendritic cells and induces their differentiation toward a Th1-polarizing phenotype. Blood 106, 946-955. (Pubitemid 41076439)
9. Varki A (2007) Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins. Nature 446, 1023-1029. (Pubitemid 46676064)
10. Wang B & Brand-Miller J (2003) The role and potential of sialic acid in human nutrition. Eur J Clin Nutr 57, 1351-1369. (Pubitemid 37407130)
11. Denhardt DT, Noda M, O'Regan AW, et al. (2001) Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J Clin Invest 107, 1055-1061. (Pubitemid 32422899)
12. Sodek J, Ganss B & McKee MD (2000) Osteopontin. Crit Rev Oral Biol Med 11, 279-303.
13. Sato T, Nakai T, Tamura N, et al. (2005) Osteopontin/Eta-1 upregulated in Crohn's disease regulates the Th1 immune response. Gut 54, 1254-1262. (Pubitemid 41192483)
14. Sodek J, Batista Da Silva AP & Zohar R (2006) Osteopontin and mucosal protection. J Dent Res 85, 404-415. (Pubitemid 43799256)
15. Agnholt J, Kelsen J, Schack L, et al. (2007) Osteopontin, a proteinwith cytokine-like properties, is associated with inflammation in Crohn's disease. Scan J Immunol 65, 453-460. (Pubitemid 46632541)
16. Scatena M, Liaw L & Giachelli CM (2007) Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler Thromb Vasc Biol 27, 2302-2309. (Pubitemid 350203943)
17. Bergelson LD (1995) Serum gangliosides as endogenous immunomodulators. Immunol Today 16, 483-486.
18. Bronnum H, Seested T, Hellgren LI, et al. (2005) Milk-derived GM(3) and GD(3) differentially inhibit dendritic cellmaturation and effector functionalities. Scand J Immunol 61, 551-557. (Pubitemid 40897111)
19. Rueda R, Maldonado J, Narbona E, et al. (1998) Neonatal dietary gangliosides. Early Hum Dev 53, S135-S147. (Pubitemid 28548708)
20. Takamizawa K, Iwamori M, Mutai M, et al. (1986) Selective changes in gangliosides of human-milk during lactation - a molecular indicator for the period of lactation. Biochim Biophys Acta 879, 73-77. (Pubitemid 16007865)
21. Martin-Sosa S, Martin MJ, Garcia-Pardo LA, et al. (2003) Sialyloligosaccharides in human and bovine milk and in infant formulas: variations with the progression of lactation. J Dairy Sci 86, 52-59. (Pubitemid 39067160)
22. Pan XL & Izumi T (2000) Variation of the ganglioside compositions of human milk, cow's milk and infant formulas. Early Hum Dev 57, 25-31. (Pubitemid 30006876)
23. Rueda R (2007) The role of dietary gangliosides on immunity and the prevention of infection. Br J Nutr 98, S68-S73. (Pubitemid 47543481)
24. Ladisch S, Becker H & Ulsh L (1992) Immunosuppression by human gangliosides: I. Relationship of carbohydrate structure to the inhibition of T cell responses. Biochim Biophys Acta Lipids Lipid Metabol 1125, 180-188.
25. Varki A (2008) Sialic acids in human health and disease. Trends Mol Med 14, 351-360.
26. Laegreid A, Otnaess ABK & Fuglesang J (1986) Human and bovine-milk - comparison of ganglioside composition and enterotoxin-inhibitory activity. Pediatr Res 20, 416-421. (Pubitemid 16117180)
27. Christensen HR, Frokiar H & Pestka JJ (2002) Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 168, 171-178. (Pubitemid 34014116)
28. Mikkelsen TL, Bakman S, Sorensen ES, et al. (2005) Sialic acid-containing milk proteins show differential immunomodulatory activities independent of sialic acid. J Agric Food Chem 53, 7673-7680. (Pubitemid 41499607)
29. Bjornvad CR, Thymann T, Deutz NE, et al. (2008) Enteral feeding induces diet-dependent mucosal dysfunction, bacterial proliferation, and necrotizing enterocolitis in preterm pigs on parenteral nutrition. Am J Physiol Gastrointest Liver Physiol 295, G1092-G1103.
30. Sangild PT, Siggers RH, Schmidt M, et al. (2006) Diet- and colonization-dependent intestinal dysfunction predisposes to necrotizing enterocolitis in preterm pigs. Gastroenterology 130, 1776-1792. (Pubitemid 43668865)
31. Van Haver ER, Oste M, Thymann T, et al. (2008) Enteral feeding reduces endothelial nitric oxide synthase in the caudal intestinal microvasculature of preterm piglets. Pediatr Res 63, 137-142.
32. De la Cochetiere MF, Piloquet H, Des Robert C, et al. (2004) Early intestinal bacterial colonization and necrotizing enterocolitis in premature infants: the putative role of Clostridium. Pediatr Res 56, 366-370. (Pubitemid 39128820)
33. Sangild PT, Bjornvad CR, Petersen YM, et al. (2002) Spontaneous NEC-like symptoms in formula-fed premature pigs. Gastroenterology 122, A278.
34. Siggers RH, Siggers J, Boye M, et al. (2008) Early administration of probiotics alters bacterial colonization and limits diet-induced gut dysfunction and severity of necrotizing enterocolitis in preterm pigs. J Nutr 138, 1437-1444.
35. Siggers RH, Thymann T, Jensen BB, et al. (2008) Elective cesarean delivery affects gut maturation and delays microbial colonization but does not increase necrotizing enterocolitis in preterm pigs. Am J Physiol Regul Integr Comp Physiol 294, R929-R938. (Pubitemid 351346972)
36. Schack L, Lange A, Kelsen J, et al. (2009) Considerable variation in the concentration of osteopontin in human milk, bovine milk, and infant formulas. J Dairy Sci 92, 5378-5385.
37. Gill HS, Doull F, Rutherfurd KJ, et al. (2000) Immunoregulatory peptides in bovine milk. Br J Nutr 84, 111-117.
38. Varki NM & Varki A (2007) Diversity in cell surface sialic acid presentations: implications for biology and disease. Lab Invest 87, 851-857. (Pubitemid 47267816)
39. Kurz G & Wallenfels K (1974) D-Galactose UV assay with galactose dehydrogenase. In Methods of Enzymatic Analysis, 2nd ed., pp. 1279-1282 [HU Bergmeyer, editor]. New York: Academic Press.
40. Thymann T, Burrin DG, Tappenden KA, et al. (2006) Formula- feeding reduces lactose digestive capacity in neonatal pigs. Br J Nutr 95, 1075-1081. (Pubitemid 43985985)
41. Sangild PT, Sjostrom H, Noren O, et al. (1995) The prenatal development and glucocorticoid control of brush-border hydrolases in the pig small-intestine. Pediatr Res 37, 207-212.
42. Oste M, Van Ginneken CJ, Van Haver ER, et al. (2005) The intestinal trophic response to enteral food is reduced in parenterally fed preterm pigs and is associated with more nitrergic neurons. J Nutr 135, 2657-2663. (Pubitemid 43156610)
43. Sangild PT, Petersen YM, Schmidt M, et al. (2002) Preterm birth affects the intestinal response to parenteral and enteral nutrition in newborn pigs. J Nutr 132, 2673-2681. (Pubitemid 35013253)
44. Buddington RK, Bering SB, Thymann T, et al. (2008) Aldohexose malabsorption in preterm pigs is directly related to the severity of necrotizing enterocolitis. Pediatr Res 63, 382-387. (Pubitemid 351450583)
45. Thymann T, Moller HK, Stoll B, et al. (2009) Carbohydrate maldigestion induces necrotizing enterocolitis in preterm pigs. Am J Physiol Gastrointest Liver Physiol 297, G1115-G1125.
46. Cilieborg MS, Boye M, Thymann T, et al. (2010) Diet-dependent effects of minimal enteral nutrition on intestinal function and necrotizing enterocolitis in preterm pigs. JPEN J Parenter Enteral Nutr (In the Press).
47. Shing CM, Peake JM, Suzuki K, et al. (2009) Bovine colostrum modulates cytokine production in human peripheral blood mononuclear cells stimulated with lipopolysaccharide and phytohemagglutinin. J Interferon Cytokine Res 29, 37-44.
48. Biswas P, Vecchi A, Mantegani P, et al. (2007) Immunomodulatory effects of bovine colostrum in human peripheral blood mononuclear cells. New Microbiol 30, 447-454. (Pubitemid 350183844)
49. Giachelli CM, Lombardi D, Johnson RJ, et al. (1998) Evidence for a role of osteopontin in macrophage infiltration in response to pathological stimuli in vivo. Am J Pathol 152, 353-358. (Pubitemid 28106380)
50. Khan SA, Lopez-Chua CA, Zhang J, et al. (2002) Soluble osteopontin inhibits apoptosis of adherent endothelial cells deprived of growth factors. J Cell Biochem 85, 728-736. (Pubitemid 34464123)
51. Xanthou G, Alissafi T, Semitekolou M, et al. (2007) Osteopontin has a crucial role in allergic airway disease through regulation of dendritic cell subsets. Nat Med 13, 570-578. (Pubitemid 46828486)
52. Da Silva APB, Pollett A, Rittling SR, et al. (2006) Exacerbated tissue destruction in DSS-induced acute colitis of OPN-null mice is associated with downregulation of TNF-alpha expression and non-programmed cell death. J Cell Physiol 208, 629-639. (Pubitemid 44141888)